Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): Age- and time-related plasticity (original) (raw)
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Pigment-Dispersing Factor-expressing neurons convey circadian information in the honey bee brain
Open Biology, 2018
Pigment-Dispersing Factor (PDF) is an important neuropeptide in the brain circadian network of Drosophila and other insects, but its role in bees in which the circadian clock influences complex behaviour is not well understood. We combined high-resolution neuroanatomical characterizations, quantification of PDF levels over the day and brain injections of synthetic PDF peptide to study the role of PDF in the honey bee Apis mellifera . We show that PDF co-localizes with the clock protein Period (PER) in a cluster of laterally located neurons and that the widespread arborizations of these PER/PDF neurons are in close vicinity to other PER-positive cells (neurons and glia). PDF-immunostaining intensity oscillates in a diurnal and circadian manner with possible influences for age or worker task on synchrony of oscillations in different brain areas. Finally, PDF injection into the area between optic lobes and the central brain at the end of the subjective day produced a consistent trend o...
Cellular and molecular mechanisms of circadian control in insects
Journal of Insect Physiology, 2001
Genetic analysis in Drosophila melanogaster has identified molecules important for the function of insect circadian clocks, and this has resulted in the elaboration of explicit biochemical models of the clock mechanism. Comparable molecular genetic analysis coupled with neuroanatomical approaches has also delineated cellular elements of the circadian pacemaker controlling insect activity rhythms. However, not much is known about the transfer of temporal information from clock cells in the insect brain to downstream neural elements or other target cells that are regulated by the clock (i.e. clock output pathways). In this review, we focus on the insect literature, with special reference to the fruitfly D. melanogaster and the hawkmoth Manduca sexta, to discuss the candidate molecules, biochemical mechanisms and cell types implicated in the clock control of behavior.
Reevaluation ofDrosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes
The Journal of Comparative Neurology, 2006
In the brain of the fly Drosophila melanogaster, ∼150 clock-neurons are organized to synchronize and maintain behavioral rhythms, but the physiological and neurochemical bases of their interactions are largely unknown. Here we reevaluate the cellular properties of these pacemakers by application of a novel genetic reporter and several phenotypic markers. First, we describe an enhancer trap marker called R32 that specifically reveals several previously undescribed aspects of the fly's central neuronal pacemakers. We find evidence for a previously unappreciated class of neuronal pacemakers, the lateral posterior neurons (LPNs), and establish anatomical, molecular, and developmental criteria to establish a subclass within the dorsal neuron 1 (DN1) group of pacemakers. Furthermore, we show that the neuropeptide IPNamide is specifically expressed by this DN1 subclass. These observations implicate IPNamide as a second candidate circadian transmitter in the Drosophila brain. Finally, we present molecular and anatomical evidence for unrecognized phenotypic diversity within each of four established classes of clock neurons.
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.
Comparative analysis of circadian clock genes in insects
Insect Molecular Biology, 2008
After a slow start, the comparative analysis of clock genes in insects has developed into a mature area of study in recent years. Brain transplant or surgical interventions in larger insects defined much of the early work in this area, before the cloning of clock genes became possible. We discuss the evolution of clock genes, their key sequence differences, and their likely modes of regulation in several different insect orders. We also present their expression patterns in the brain, focusing particularly on Diptera, Lepidoptera, and Orthoptera, the most common non-genetic model insects studied. We also highlight the adaptive involvement of clock molecules in other complex phenotypes which require biological timing, such as social behaviour, diapause and migration.
Journal of Biological Rhythms, 2015
Homologous circadian genes are found in all insect clocks, but their contribution to species-specific circadian timing systems differs. The aim of this study was to extend research within Lepidoptera to gain a better understanding of the molecular mechanism underlying circadian clock plasticity and evolution. The Mediterranean flour moth, Ephestia kuehniella (Pyralidae), represents a phylogenetically ancestral lepidopteran species. We have identified circadian rhythms in egg hatching, adult emergence, and adult locomotor activity. Cloning full-length complementary DNAs and further characterization confirmed one copy of period and timeless genes in both sexes. Both per and tim transcripts oscillate in their abundance in E. kuehniella heads under light-dark conditions. PER-like immunoreactivity (PER-lir) was observed in nuclei and cytoplasm of most neurons in the central brain, the ventral part of subesophageal complex, the neurohemal organs, the optic lobes, and eyes. PER-lir in photoreceptor nuclei oscillated during the day with maximal intensity in the light phase of the photoperiodic regime and lack of a signal in the middle of the dark phase. Expression patterns of per and tim messenger RNAs (mRNAs) were revealed in the identical location as the PER-lir was detected. In the photoreceptors, a daily rhythm in the intensity of expression of both per mRNA and tim mRNA was found. These findings suggest E. kuehniella as a potential lepidopteran model for circadian studies.
Insect timing (rhythms) from the point of view of neuroendocrine effector mechanisms
Acta Phytopathologica et Entomologica Hungarica, 2009
Living organisms, including insects, have developed a complex array of physiological and behavioral mechanisms allowing them to cope with biotic and abiotic challenges. Under natural circumstances they are readily capable to make 'predictions' and consequently can adjust their physiology and behavior to 'anticipate' the expected changes. The compilation of predictions provide a fine tuning to prepare for would-be conditions allowing them to react at the right time by the best set of available physiological, behavioral 'answers'. The attained internal harmony of the organism is the best option what an individual may achieve. Among insects, the most significant controller of rhythms is light and its changes, while temperature, humidity, food availability and population densities are also important. Rhythmic events at individual and population levels may be grouped as follows: development, dormant, reproductive, behavioral, metabolic cycles and polymorphism. The periodic changing of light and biological events related to this provides the most elaborate model. The main elements are: photoreception; clock mechanism measuring day and/or night length; photoperiodic counter including memory to accumulate information; neuroendocrine effector mechanisms regulating relevant physiological processes. A description of elements and an inventory will be provided of respective hormones, neuropeptides which are notably taking part in controlling events.
Journal of Comparative Physiology B, 2012
Many physiological functions of insects show a rhythmic change to adapt to daily environmental cycles. These rhythms are controlled by a multi-clock system. A principal clock located in the brain usually organizes the overall behavioral rhythms, so that it is called the ''central clock''. However, the rhythms observed in a variety of peripheral tissues are often driven by clocks that reside in those tissues. Such autonomous rhythms can be found in sensory organs, digestive and reproductive systems. Using Drosophila melanogaster as a model organism, researchers have revealed that the peripheral clocks are self-sustained oscillators with a molecular machinery slightly different from that of the central clock. However, individual clocks normally run in harmony with each other to keep a coordinated temporal structure within an animal. How can this be achieved? What is the molecular mechanism underlying the oscillation? Also how are the peripheral clocks entrained by light-dark cycles? There are still many questions remaining in this research field. In the last several years, molecular techniques have become available in nonmodel insects so that the molecular oscillatory mechanisms are comparatively investigated among different insects, which give us more hints to understand the essential regulatory mechanism of the multi-oscillatory system across insects and other arthropods. Here we review current knowledge on arthropod's peripheral clocks and discuss their physiological roles and molecular mechanisms. Keywords Circadian clock Á Clock gene Á Peripheral clock Á Molecular oscillation Á Entrainment Communicated by I.D. Hume.
Cell and Tissue Research, 1999
The accessory medulla with its associated pigment-dispersing hormone-immunoreactive neurons appears to be the pacemaker that controls the circadian locomotor activity rhythm of the cockroach Leucophaea maderae. To permit studies at the level of individual, identified, pacemaker neurons, we developed specific long-term primary cell cultures of fully differentiated adult neurons of the accessory medulla. As judged from soma diameter distribution, the cultures contain an unbiased representation of apparently all neuronal types of the accessory medulla. The cultured cells survive and grow processes for more than 2 months with or without additional hemocyte coculturing. However, a strong positive effect on initial outgrowth was observed with hemocyte coculturing. At least six different morphological cell types of the accessory medulla could be distinguished in vitro. Among these only one cell type, the monopolar type C cell, was recognized in vitro with an antiserum against the neuropeptide pigment-dispersing hormone. Thus, the identifiable monopolar type C cells are candidates for circadian pacemaker neurons and will be the focus of further physiological characterizations.
Daily rhythms in cells of the fly's optic lobe: taking time out from the circadian clock
Trends in Neurosciences, 1996
Considerable progress has recently been reported in locating the cellular basis and molecular mechanisms of the circadian clock in the fruitfly, Drosophila melanogaster.To advance beyond the clock, towards the outputs that lie between the clock itself and the circadian rhythms in behaviour that it regulates, will present new challenges.This is because most behaviours are generated by complex neuronal circuits,which are themselves difficult to unravel.Recently described anatomical changes in the optic lobe of the related housefly, Musca domestica, exhibit a circadian rhythm that is, by contrast, relatively easy to assay.This rhythm is apparently controlled by at least two sets of diffuse modulatory neurones. One of these, immunoreactive to the peptide pigment-dispersing hormone,also expresses in Drosophila the product of the period (per) gene,the most widely studied of the so-called clock genes that are essential for the correct expression of circadian rhythmicity. The second, called LBO5HT, is immunoreactive to 5-HT, a widely invoked transmitter system in insect circadian rhythms.The identification of these elements, and a widening cascade of events which their actions apparently trigger, opens up new opportunities to examine old problems in the regulation of circadian rhythms in the nervous system.