Daily rhythm of responsiveness to prothoracicotropic hormone in prothoracic glands ofRhodnius prolixus (original) (raw)
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General and Comparative Endocrinology, 1996
A daily rhythm of release of prothoracicotropic hor-and consequently imposes temporal order on ecdysteroid-dependent developmental events. ᭧ 1996 Academic mone (PTTH) has been reported throughout most of larval -adult development in Rhodnius prolixus. PTTH Press, Inc. released by explanted brain-retrocerebral complexes was quantified using an in vitro bioassay in which the Prothoracicotropic hormone (PTTH) plays a pivotal PTTH released into the incubation medium was asrole in the regulation of insect development (Bollensayed by its ability to stimulate ecdysteroid synthesis bacher and Gilbert, 1981; Bollenbacher and Granger, in arrhythmic prothoracic glands (PGs). The present 1985). This cerebral neuropeptide is released from the article employs this assay to reveal that the daily retrocerebral complex (corpus cardiacum plus corpus rhythm of PTTH release is under circadian control.
General and Comparative Endocrinology, 1991
Rhythmic synthesis of moulting hormones (ecdysteroids) by prothoracic glands (PGs) of the insect Rhodnius prolixus during the last larval instar was studied in vitro following explantations every 4-5 hr for up to 96 hr. Ecdysteroid synthesis was measured by radioimmunoassay as the quantity of ecdysteroid produced during 4 hr in vitro. A massive daily rhythm is seen, with synthesis at night being three-to fivefold higher than during the day. This rhythm of ecdysteroid synthesis by PGs free-runs in continuous darkness with a temperature-compensated period length close to 24 hr and is therefore controlled by a circadian system. This is the first report of circadian regulation of synthesis of an invertebrate hormone. The synthesis rhythm also free-runs in continuous light, but with an inverted phase and shorter period length. It is argued that the circadian system controlling synthesis comprises two oscillators which free-run in antiphase, occupy different anatomical locations, and are coupled by a humoral factor, possibly prothoracicotropic hormone. The ecdysteroid synthesis rhythm in PGs appears to drive the previously reported circadian rhythm in the haemolymph ecdysteroid titre. It is concluded that the circadian system controlling synthesis of ecdysteroids constitutes a pacemaker which drives various rhythms in the target cells of ecdysteroids via the rhythm in the haemolymph titre. Ecdysteroids are viewed as "hormonal Zeitgebers. " imposing temporal order on development. 10
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2012
Prothoracicotropic hormone (PTTH) is a brain neurohormone that has been studied for over 80 years. The only known target of PTTH is the prothoracic glands (PGs) of larvae, which synthesize the insect molting hormones (ecdysteroids) and a massive literature exists on this axis. The PGs degenerate around the time of adult emergence, yet presence of PTTH has been reported in the brains of several adult insects. Using an in vitro bioassay system, we confirm that PTTH is present in the adult female brain of Rhodnius prolixus. The material is electrophoretically, immunologically and biologically indistinguishable from larval PTTH. The amount of PTTH in the brain shows a daily rhythm during egg development. We show that brains in vitro release PTTH with a daily rhythm over this period of time. PTTH is released at each scotophase. This is the first report that PTTH is released from the adult brain and functions as a hormone, inviting explanation of its function. Larval PTTH is also known to be released with a daily rhythm, and the clock in the brain controls both larval and adult rhythms. The potential significance of rhythmic PTTH release in female adults is discussed in relation to the regulation of ecdysteroids, egg development and the concept of internal temporal order.
Journal of Insect Physiology, 2001
Circadian rhythms have been described in Rhodnius prolixus in both the release of prothoracicotropic hormone (PTTH) from the brain complex and the synthesis (and release) of ecdysteroids by the prothoracic glands (PGs). The PGs possess a circadian oscillator that is light-sensitive in vitro. The present work reports the ability of a 'lights-off' signal to induce rhythmicity in both PTTH and ecdysteroids in whole animals. Continuous light (LL) caused cessation of release of PTTH; rhythmic release was promptly initiated by transfer to darkness (DD). We infer a light-sensitive circadian oscillator that regulates PTTH release and discuss evidence of its location in the protocerebrum. PGs maintained in LL became arrhythmic but maintained a developmental modulation of steroidogenesis. Transfer of animals to DD initiated rhythmic steroidogenesis; thus, the 'PG oscillator' operates in vivo despite an overlying cuticle. The first initiated peak in steroidogenesis precedes that of PTTH by several hours and was not impaired when PTTH release was prevented by prior injection of tetrodotoxin. In normal animals (PTTH present), the phase of the induced rhythm of steroidogenesis was shifted in a single cycle to align with that of PTTH release. We conclude that both 'brain oscillator' and 'PG oscillator' are photosensitive, and the induced PTTH rhythm regulates the phase of rhythmic steroidogenesis. This neuroendocrine axis contains (at least) three photosensitive oscillators, in which classical pacemaker and slave oscillators are not obvious. Caution in the application of formal terminology to discrete tissues is urged. This multioscillator timing system appears to direct the circadian organization of development through the rhythm in haemolymph ecdysteroids that reaches ecdysone-responsive cells.
General and Comparative Endocrinology, 1989
The synthesis of ecdysteroids by prothoracic glands (PGs) of male last instar larvae of Rhodnius prolixus was measured in vitro by radioimmunoassay throughout the course of larval-adult development. Large and systematic changes in relative rates of synthesis occur during development. Two bursts of elevated synthetic activity were found. The first commences as soon as development is initiated by a blood meal and lasts approximately 1 day. The second commences 4 days later and increases progressively to a peak at Days 11-13 after feeding (up to 25 ng of 20-hydroxyecdysone eq. gland-1/4 hr-1). The onset of each of these bursts of activity coincides with apparent times of PG stimulation in vivo by release of the prothoracicotropic hormone from the brain. Both bursts result in increases in hemolymph ecdysteroid titer measured in the donor animals. PGs exhibit an abrupt attenuation of synthesis on Day 14, which is followed by a rapid decline in the hemolymph ecdysteroid titer. Clearly, ecdysteroid synthesis by PGs is a major factor regulating the hemolymph titer.
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1998
The paired prothoracic glands of the insect Rhodnius prolixus each comprise a group of about 200 structurally identical cells. The synthesis (and release) of steroid moulting hormones (ecdysteroids) by these glands is under circadian control in vivo. We monitored ecdysteroid synthesis by single glands during long-term incubations in vitro. Synthesis is rhythmic in vitro and persists in continuous darkness. Glands which are arrhythmic (from prolonged continuous light) respond to transfer to darkness in vitro with the initiation of a freerunning circadian rhythm of ecdysteroid synthesis. Therefore, the glands possess a light-sensitive circadian oscillator. These properties are conventionally associated with nervous tissue of animals. It is suggested that rhythmicity is synchronized within the gland by the known structural and electrical coupling between its component cells. The glands share properties with known pacemakers such as the avian pineal. However, the glands in vivo receive input from both light cues and the cerebral neuropeptide, prothoracicotropic hormone. Rhythmic release of this neuropeptide is controlled by a second oscillator located in the brain. We conclude that the pacemaker in the endocrine system of R. prolixus comprises at least three oscillators, one in each prothoracic gland and one in the brain, which are coupled hormonally. We conclude that the prothoracic gland is an important component of the circadian system controlling development in R. prolixus and that peripheral endocrine glands may play a more active role in the generation of animal circadian organization than has been thought.
The Journal of Comparative Neurology, 2007
This paper reports the localization in the Rhodnius prolixus brain of neurons producing the key neuropeptide that regulates insect development, prothoracicotropic hormone (PTTH) and describes intimate associations of the PTTH neurons with the brain circadian timekeeping system. Immunohistochemistry and confocal laser scanning microscopy revealed that the PTTH-positive neurons in larvae are located in a single group in the lateral protocerebrum. Their number increases from two in the last larval instar to five during larval-adult development. In adults, there are two distinct groups of these neurons composed of two cells each. A daily rhythm in content of PTTH-positive material occurs in both the somata and the axons in both larval and adult stages. These rhythms correlate with previous evidence of a circadian rhythm of PTTH release from brains in vitro. The key circadian clock cells of Rhodnius are eight neurons, which co-express pigment-dispersing factor (PDF) and the canonical clock proteins PER and TIM; PDF fills the axons. Equivalent cells control behavioral rhythms in other insects. Double labeling revealed intimate associations between axons of larval PTTH neurons and clock neurons, indicating a neuronal pathway from the brain timekeeping system for circadian control of PTTH release. Additional PDF neurons appear in the adult, associated with the second group of PTTH neurons. These findings provide the first direct evidence that neurons of the insect brain timekeeping system control hormone rhythms. The range of functions regulated by this timekeeping system is quite similar to those of the vertebrate suprachiasmatic nucleus, for which the insect system is a valuable model. J. Comp. Neurol. 503:511-524, 2007. All multicellular organisms possess internal timing mechanisms (circadian systems) that function to orchestrate the myriad physiological and biochemical events within the organism both with respect to each other and with respect to external time. Thus circadian systems exploit the reliability of signals from the external world (mainly light cues) to organize internal events. This internal temporal organization is critical for survival, because its breakdown (in aperiodic or noncircadian environments) leads to premature death in insects and health problems in human shift workers and frequent sufferers of jet-lag . The mechanisms that generate and distribute this internal temporal organization have been studied in detail only in mammals and insects. In mam-mals, the circadian system is composed of multiple coupled circadian oscillators in the paired suprachiasmatic nuclei (SCN), pineal organ, and ocular retinae (Ikonomov et al.
Cell and Tissue Research, 2006
The insect moulting hormones, viz. the ecdysteroids, regulate gene expression during development by binding to an intracellular protein, the ecdysteroid receptor (EcR). In the insect Rhodnius prolixus, circulating levels of ecdysteroids exhibit a robust circadian rhythm. This paper demonstrates associated circadian rhythms in the abundance and distribution of EcR in several major target tissues of ecdysteroids, but not in others. Quantitative analysis of immunofluorescence images obtained by confocal laserscanning microscopy following the use of anti-EcR has revealed a marked daily rhythm in the nuclear abundance of EcR in cells of the abdominal epidermis, brain, fat body, oenocytes and rectal epithelium of Rhodnius. This EcR rhythm is synchronous with the rhythm of circulating hormone levels. It free-runs in continuous darkness for several cycles, showing that EcR nuclear abundance is under circadian control. Circadian control of a nuclear receptor has not been shown previously in any animal. We infer that the above cell types detect and respond to the temporal signals in the rhythmic ecdysteroid titre. In several cell types, the rhythm in cytoplasmic EcR peaks several hours prior to the EcR peak in the nucleus each day, thereby implying a daily migration of EcR from the cytoplasm to the nucleus. This finding shows that EcR is not a constitutive nuclear receptor, as has previously been assumed. In the brain, rhythmic nuclear EcR has been found in peptidergic neurosecretory cells, indicating a potential pathway for feedback regulation of the neuroendocrine system by ecdysteroids, and also in regions containing circadian clock neurons, suggesting that the circadian timing system in the brain is also sensitive to rhythmic ecdysteroid signals.