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Biomedical subjects

J W Truman

Publications and source records attributed to J W Truman.

At least 19 recordsLinked to original sources
PubMed2001

Tiling of the body wall by multidendritic sensory neurons in Manduca sexta.

A plexus of multidendritic sensory neurons, the dendritic arborization (da) neurons, innervates the epidermis of soft-bodied insects. Previous studies have indicated that the plexus may comprise distinct subtypes of da neurons, which utilize diverse cyclic 3',5'-guanosine monophosphate signaling pathways and could serve several functions. Here, we identify three distinct classes of da neurons in Manduca, which we term the alpha, beta, and gamma classes. These three classes differ in their sensory responses, branch complexity, peripheral dendritic fields, and axonal projections. The two identified alpha neurons branch over defined regions of the body wall, which in some cases correspond to specific natural folds of the cuticle. These cells project to an intermediate region of the neuropil and appear to function as proprioceptors. Three beta neurons are characterized by long, sinuous dendritic branches and axons that terminate in the ventral neuropil. The function of this group of neurons is unknown. Four neurons belonging to the gamma class have the most complex peripheral dendrites. A representative gamma neuron responds to forceful touch of the cuticle. Although the dendrites of da neurons of different classes may overlap extensively, cells belonging to the same class show minimal dendritic overlap. As a result, the body wall is independently tiled by the beta and gamma da neurons and partially innervated by the alpha neurons. These properties of the da system likely allow insects to discriminate the quality and location of several types of stimuli acting on the cuticle.

Animals↗
PubMed2001

Soluble guanylate cyclase is required during development for visual system function in Drosophila.

A requirement for nitric oxide (NO) in visual system development has been demonstrated in many model systems, but the role of potential downstream effector molecules has not been established. Developing Drosophila photoreceptors express an NO-sensitive soluble guanylate cyclase (sGC), whereas the optic lobe targets express NO synthase. Both of these molecules are expressed after photoreceptor outgrowth to the optic lobe, when retinal growth cones are actively selecting their postsynaptic partners. We have previously shown that inhibition of the NO-cGMP pathway in vitro leads to overgrowth of retinal axons. Here we examined flies mutant for the alpha subunit gene of the Drosophila sGC (Gcalpha1). This mutation severely reduced but did not abolish GCalpha1 protein levels and NO-stimulated sGC activity in the developing photoreceptors. Although few mutant individuals possessed a disorganized retinal projection pattern, pharmacological NOS inhibition during metamorphosis increased this disorganization in mutants to a greater degree than in the wild type. Adult mutants lacked phototactic behavior, and the off-transient component of electroretinograms was frequently absent or greatly reduced in amplitude. Normal phototaxis and off-transient amplitude were restored by heat shock-mediated Gcalpha1 expression applied during metamorphosis but not in the adult. We propose that diminished sGC activity in the visual system during development causes inappropriate or inadequate formation of first-order retinal synapses, leading to defects in visual system function and visually mediated behavior.

Animals↗
PubMed2001

Neural network partitioning by NO and cGMP.

The stomatogastric ganglion (STG) of the crab Cancer productus contains approximately 30 neurons arrayed into two different networks (gastric mill and pyloric), each of which produces a distinct motor pattern in vitro. Here we show that the functional division of the STG into these two networks requires intact NO-cGMP signaling. Multiple nitric oxide synthase (NOS)-like proteins are expressed in the stomatogastric nervous system, and NO appears to be released as an orthograde transmitter from descending inputs to the STG. The receptor of NO, a soluble guanylate cyclase (sGC), is expressed in a subset of neurons in both motor networks. When NO diffusion or sGC activation are blocked within the ganglion, the two networks combine into a single conjoint circuit. The gastric mill motor rhythm breaks down, and several gastric neurons pattern switch and begin firing in pyloric time. The functional reorganization of the STG is both rapid and reversible, and the gastric mill motor rhythm is restored when the ganglion is returned to normal saline. Finally, pharmacological manipulations of the NO-cGMP pathway are ineffective when descending modulatory inputs to the STG are blocked. This suggests that the NO-cGMP pathway may interact with other biochemical cascades to partition rhythmic motor output from the ganglion.

Animals↗
PubMed2000

Ecdysteroid coordinates optic lobe neurogenesis via a nitric oxide signaling pathway.

Proliferation of neural precursors in the optic lobe of Manduca sexta is controlled by circulating steroids and by local production of nitric oxide (NO). Diaphorase staining, anti-NO synthase (NOS) immunocytochemistry and the NO-indicator, DAF-2, show that cells throughout the optic anlage contain NOS and produce NO. Signaling via NO inhibits proliferation in the anlage. When exposed to low levels of ecdysteroid, NO production is stimulated and proliferation ceases. When steroid levels are increased, NO production begins to decrease within 15 minutes independent of RNA or protein synthesis and cells rapidly resume proliferation. Resumption of proliferation is not due simply to the removal of NO repression though, but also requires an ecdysteroid stimulatory pathway. The consequence of these opposing pathways is a sharpening of the responsiveness to the steroid, thereby facilitating a tight coordination between development of the different elements of the adult visual system.

Animals↗
PubMed2000

The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids.

The steroid hormone 20-hydroxyecdysone (20E) initiates metamorphosis in insects by signaling through the ecdysone receptor complex, a heterodimer of the ecdysone receptor (EcR) and ultraspiracle (USP). Analysis of usp mutant clones in the wing disc of Drosophila shows that in the absence of USP, early hormone responsive genes such as EcR, DHR3 and E75B fail to up-regulate in response to 20E, but other genes that are normally expressed later, such as (&bgr;)-Ftz-F1 and the Z1 isoform of the Broad-Complex (BRC-Z1), are expressed precociously. Sensory neuron formation and axonal outgrowth, two early metamorphic events, also occur prematurely. In vitro experiments with cultured wing discs showed that BRC-Z1 expression and early metamorphic development are rendered steroid-independent in the usp mutant clones. These results are consistent with a model in which these latter processes are induced by a signal arising during the middle of the last larval stage but suppressed by the unliganded EcR/USP complex. Our observations suggest that silencing by the unliganded EcR/USP receptor and the subsequent release of silencing by moderate steroid levels may play an important role in coordinating early phases of steroid driven development.

Animals↗
PubMed1999

Regulation of cyclic GMP elevation in the developing antennal lobe of the Sphinx moth, Manduca sexta.

In the moth, Manduca sexta, 3',5'-guanosine monophosphate (cGMP) is transiently elevated during adult development in about 100 neurons of the antennal lobe. We demonstrate that nearly all of these neurons are local interneurons of the lateral cluster I, that their capacity to show a strong cGMP response during development is regulated by the steroid hormone 20-hydroxyecdysone, and that in a subpopulation of these neurons cGMP elevation seems to be controlled directly by the gaseous messenger molecule nitric oxide (NO). Treatment with the acetylcholine esterase inhibitor eserine, antennal nerve transection, and electrical stimulation of the antennae suggest that NO/cGMP signaling during development is an activity-dependent process. Besides input from the antennae, input from the central brain and the ventral ganglia is involved in upregulating cGMP in the antennal-lobe neurons. Possible sources are centrifugal aminergic neurons, since application of serotonin and histamine enhances the GMP signal in local interneurons. Comparing the time course of cGMP elevation with events occurring during development leads us to the hypothesis that the NO/cGMP signaling pathway might be involved in synapse formation of a subset of antennal-lobe neurons.

Animals↗
PubMed1999

The origins of insect metamorphosis.

Insect metamorphosis is a fascinating and highly successful biological adaptation, but there is much uncertainty as to how it evolved. Ancestral insect species did not undergo metamorphosis and there are still some existing species that lack metamorphosis or undergo only partial metamorphosis. Based on endocrine studies and morphological comparisons of the development of insect species with and without metamorphosis, a novel hypothesis for the evolution of metamorphosis is proposed. Changes in the endocrinology of development are central to this hypothesis. The three stages of the ancestral insect species-pronymph, nymph and adult-are proposed to be equivalent to the larva, pupa and adult stages of insects with complete metamorphosis. This proposal has general implications for insect developmental biology.

Animals↗
PubMed1999

Development and organization of a nitric-oxide-sensitive peripheral neural plexus in larvae of the moth, Manduca sexta.

Each hemisegment of the Manduca sexta larva is supplied with a subepidermal plexus of approximately 350 multidendritic neurons. An initial set of neurons, the primary plexus neurons, arise at 35-45% of embryogenesis. These neurons comprise 12-16 uniquely identifiable neurons per hemisegment that have homologues in other insect larvae. Each spreads processes across a characteristic portion of the body wall and has an axon that projects into the central nervous system. Secondary plexus neurons are born in two waves: the first between 70% and 80% of embryogenesis and the second during the molt to the second larval stage. The secondary plexus neurons are multidendritic, spread uniformly across the body wall, and appear to make contacts with the primary plexus neurons. Each secondary plexus cell arises as part of a five-cell cluster; the other cells produce a sensory bristle and socket along with the bristle sensory neuron and a glial cell. Application of nitric oxide (NO) donors induces plexus neurons to produce cyclic 3',5' guanosine monophosphate (cGMP), suggesting the presence of soluble guanylate cyclase. With few exceptions, plexus neurons become sensitive to NO stimulation approximately 10 hours after their birth and remain so throughout larval life. Cyclic GMP is detected primarily in the cytoplasm of plexus neurons and extends into the finest peripheral dendrites. Our results suggest that cGMP participates in the development and/or physiology of this peripheral neural plexus.

Animals↗
PubMed1999

Hormonal control of ventral diaphragm myogenesis during metamorphosis of the moth, Manduca sexta.

Both the proliferation and differentiation of ventral diaphragm myoblasts are controlled by ecdysteroid during metamorphosis of the moth, Manduca sexta, but the responses have different hormonal requirements. Tonic exposure to moderate levels of ecdysteroid are required to stimulate myoblast proliferation. This is due to the presence of an ecdysteroid-dependent control point in the G(2) phase of the cell cycle. As a result, proliferation can be repeatedly turned on or off simply by adjusting the concentration of ecdysteroid to be above or below a critical threshold concentration. In contrast, high levels of ecdysteroid trigger irreversible proliferative arrest and differentiation of myofibers. Myoblast proliferation and differentiation also differ in their response to the juvenile hormone mimic, methoprene. Ecdysteroid-dependent proliferative arrest and differentiation are blocked by coculture with methoprene but methoprene has no effect on ecdysteroid-dependent proliferation. In the animal, premature exposure to high levels of ecdysteroid in the absence of juvenile hormone triggers precocious differentiation of the myoblasts, resulting in the formation of several thin bands of muscle rather than a complete diaphragm. Thus, ecdysteroid and juvenile hormone collaborate to determine the size and shape of the adult musculature.

Animals↗
PubMed1999

The sequence of Locusta RXR, homologous to Drosophila Ultraspiracle, and its evolutionary implications.

The cellular response to steroid hormones is mediated by nuclear receptors which act by regulating transcription. In Drosophila melanogaster, the receptor for the insect molting hormone, 20-hydroxyecdysone, is a heterodimer composed of the Ecdysone Receptor and Ultraspiracle (USP) proteins. The DNA binding domains of arthropod USPs and their vertebrate homologs, the retinoid X receptor (RXR) family, are highly conserved. The ligand binding domain sequences, however, divide into two distinct groups. One group consists of sequences from members of the holometabolous higher insect orders Diptera and Lepidoptera, the other of sequences from vertebrates, a crab and a tick. We here report the sequence of an RXR/USP from the hemimetabolous orthopteran, Locusta migratoria. The locust RXR/USP ligand binding domain clearly falls in the vertebrate-crab-tick rather than the dipteran-lepidopteran group. The reason for the evolutionarily abrupt divergence of the dipteran and lepidopteran sequences is unknown, but it could be a change in the type of ligand bound or the loss of ligand altogether.

Amino Acid Sequence↗
PubMed1999

The hormonal coordination of behavior and physiology at adult ecdysis in Drosophila melanogaster.

In insects, ecdysis is thought to be controlled by the interaction between peptide hormones; in particular between ecdysis-triggering hormone (ETH) from the periphery and eclosion hormone (EH) and crustacean cardioactive peptide (CCAP) from the central nervous system. We examined the behavioral and physiological functions of the first two of these peptides in Drosophila melanogaster using wild-type flies and knockout flies that lacked EH neurons. We used ETH from Manduca sexta (MasETH) to induce premature ecdysis and compared the responses of the two types of flies. The final release of EH normally occurs approximately 40 min before ecdysis. It is correlated with cyclic guanosine monophosphate (cGMP) production in selected neurons and tracheae, by an elevation in the heart rate and by the filling of the new tracheae with air. Injection of developing flies with MasETH causes all these events to occur prematurely. In EH cell knockouts, none of these changes occurs in response to MasETH, and these flies show a permanent failure in tracheal filling. This failure can be overcome in the knockouts by injecting them with membrane-permeant analogs of cGMP, the second messenger for EH. The basis for the 40 min delay between EH release and the onset of ecdysis was examined by decapitating flies at various times relative to EH release. In flies that had already released EH, decapitation was always followed within 1 min by the start of ecdysis. Immediate ecdysis was never observed when the EH cell knockout flies were decapitated. We propose that EH activates both ventral central nervous system elements necessary for ecdysis (possibly the CCAP cells) and descending inhibitory neurons from the head. This descending inhibition establishes a delay in the onset of ecdysis that allows the completion of EH-activated physiological processes such as tracheal filling. A waning in the inhibition eventually allows ecdysis to begin 30-40 min later.

Animals↗
PubMed1999

Eclosion hormone provides a link between ecdysis-triggering hormone and crustacean cardioactive peptide in the neuroendocrine cascade that controls ecdysis behavior.

Three insect peptide hormones, eclosion hormone (EH), ecdysis-triggering hormone (ETH) and crustacean cardioactive peptide (CCAP), have been implicated in controlling ecdysis behavior in insects. This study examines the interactions between these three peptides in the regulation of the ecdysis sequence. Using intracellular recordings, we found that ETH is a potent activator of the EH neurons, causing spontaneous action potential firing, broadening of the action potential and an increase in spike peak amplitude. In turn, electrical stimulation of the EH neurons or bath application of EH to desheathed ganglia resulted in the elevation of cyclic GMP (cGMP) levels within the Cell 27/704 group (which contain CCAP). This cGMP production increases the excitability of these neurons, thereby facilitating CCAP release and the generation of the ecdysis motor program. Extracellular recordings from isolated nervous systems show that EH has no effect on nervous systems with an intact sheath. In desheathed preparations, in contrast, EH causes only the ecdysis motor output. The latency from EH application to ecdysis was longer than that after CCAP application, but shorter than that when ETH is applied to a whole central nervous system. These data, along with previously published results, support a model in which ETH causes pre-ecdysis behavior and at higher concentrations stimulates the EH neurones. EH release then facilitates the onset of ecdysis by enhancing the excitability of the CCAP neurons.

Animals↗
PubMed1998

Programmed cell death of identified peptidergic neurons involved in ecdysis behavior in the Moth, Manduca sexta.

The eclosion of the adult Manduca sexta moth is followed by a wave of cell death that eliminates up to 50% of the neurons of the central nervous system within the first few days of imaginal life. While the identity of some of the dying motoneurons has been established, that of most doomed neurons is unknown. Here, we show that the dying cells include peptidergic neurons involved in the control of ecdysis behavior. These cells belong to a small population of 50 neurons that express crustacean cardioactive peptide (CCAP), a potent regulator of the ecdysis motor program, and show increases in cyclic 3',5'-guanosine monophosphate at each ecdysis. First, we describe new markers for these neurons and show that they are expressed in these CCAP-immunoreactive neurons in a complex temporal pattern during development. We then show that these neurons die within 36 h after adult eclosion, the last performance of ecdysis behavior in the life of the animal, via the active, genetically determined process of programmed cell death. The death of these neurons supports the hypothesis that outmoded or unused neurons are actively eliminated.

Animals↗
PubMed1998

Distribution of GABA-like immunoreactive neurons in insects suggests lineage homology.

Gamma-aminobutyric acid (GABA) is an important inhibitory neurotransmitter in vertebrates and invertebrates (Sattelle [1990] Adv. Insect Physiol. 22:1-113). The GABA phenotype is lineally determined in postembryonic neurons in the tobacco hawkmoth, Manduca sexta (Witten and Truman, [1991] J. Neurosci. 11:1980-1989) and is restricted to six identifiable postembryonic lineages in the moth's thoracic hemiganglia. We used a comparative approach to determine whether this distinct clustering of GABAergic neurons is conserved in Insecta. In the nine orders of insects surveyed (Thysanura, Odonata, Orthoptera, Isoptera, Hemiptera, Coleoptera, Diptera, Lepidoptera, and Hymenoptera), GABA-like immunoreactive neurons within a thoracic hemiganglion were clustered into six distinct groups that occupied positions similar to the six postembryonic lineages in Manduca. On the basis of cell body position and axon trajectories, we suggest that these are indeed homologous lineage groups and that the lineal origins of the GABAergic cells have been very conservative through insect evolution. The distinctive clustering of GABA-positive cells is shared with crustaceans (Mulloney and Hall [1990] J. Comp. Neurol. 291:383-394; Homberg et al. [1993] Cell Tissue Res. 271:279-288) but is not found in the centipede Lithobius forficulatus. There is a two- to threefold increase in numbers of thoracic neurons between the flightless Thysanura and the most advanced orders of insects. Using the GABA clusters as indicators of specific lineages, we find that only selected lineages have significantly contributed to this increase in neuronal numbers.

Animals↗
PubMed1998

Metamorphic control of cyclic guanosine monophosphate expression in the nervous system of the tobacco hornworm, Manduca sexta.

During metamorphosis of Manduca sexta, defined sets of neurons show a dramatic accumulation of cyclic guanosine monophosphate (cGMP). Although many of these cells show low but detectable levels of cGMP during specific developmental windows, these levels are enhanced dramatically during dissection of the central nervous system (CNS). The ability of these neurons to show this induced cGMP expression depends on the developmental stage. Larvae do not show this capacity but it appears during the transition from the larval to the pupal stage. There are two different classes of response: the early expressing neurons start to show a cGMP response at the beginning of the prepupal stage while the late expressing cGMP neurons start at different times during the pupal-adult transition. The former set includes larval neurons that will likely be remodeled during metamorphosis, and a number of them are serotonergic. The late-expressing group also includes some larval cells, but most are adult-specific neurons. At least for one adult-specific cluster, the antennal lobe neurons, the cGMP expression parallels the maturation phase of these cells.

Animals↗
PubMed1998

Developing grasshopper neurons show variable levels of guanylyl cyclase activity on arrival at their targets.

The ability of certain grasshopper neurons to respond to exogenously applied donors of nitric oxide (NO) by producing cyclic GMP (cGMP) depends on their developmental state. ODQ, a selective blocker of NO-sensitive guanylyl cyclase, blocks cGMP production at 10(-5) M, thus confirming the nature of the response. Experiments in which the distal axon is separated from its proximal stump before application of an NO donor show that guanylyl cyclase is distributed uniformly throughout the neuron. In the locust abdomen, where segments are formed sequentially, the pattern of guanylyl cyclase up-regulation is predictable and sequential from anterior to posterior. There are two patterns of innervation by cGMP-expressing motor neurons. In the first, typified by muscle 187, an innervating neuron begins to be NO responsive on arrival at its muscle and continues to be so over most of the remainder of embryonic development, including the formation of motor end plates. In the second, typified by a neuron innervating muscle 191, the neuron extends well along the muscle, apparently laying down a number of sites of contact with it, before it becomes NO responsive. In both patterns, however, NO responsiveness marks the neuron's transition from growth cone elongation to the production of lateral branches. Individual muscles receive innervation from multiple motor neurons, some of which express transient NO sensitivity during development and others which do not. With the exception of the leg motor neuron SETi, the first motor neuron to reach any muscle is usually not NO responsive. We suggest that cGMP plays a role in, or reflects, the early stages of communication between a target and specific innervating neurons.

Animals↗
PubMed1998

Steroid and neuronal regulation of ecdysone receptor expression during metamorphosis of muscle in the moth, Manduca sexta.

Ecdysteroids regulate the remodeling of the dorsal external oblique 1 (DEO1) muscle during metamorphosis in Manduca sexta (). We show that the temporal and spatial patterning of the A and B1 isoforms of the ecdysone receptor (EcR) within muscle DEO1 corresponds with the developmental fates of the fibers. Using antibodies directed to specific isoforms of EcR, we show that the expression of various EcR isoforms in myonuclei differ among the five fibers of DEO1 and correspond with the developmental response of the muscle to the changing steroid titers and to the pattern of innervation. Muscle degeneration and apoptosis of myonuclei in all fibers are correlated with the expression of only EcR-A just before pupal ecdysis and then with the expression of low levels of both EcR-A and EcR-B1 shortly after pupation. Only the first fiber of muscle DEO1 participates in the regrowth of the adult muscle, and only this fiber shows an upregulation of EcR-B1 that is evident at 3 d after pupal ecdysis. Denervation of the muscle prevents both the upregulation of EcR-B1 and myoblast proliferation. We conclude that the developmental fate of muscle DEO1 during metamorphosis is orchestrated by interactions between rising and falling ecdysteroid titers, the pattern of expression of EcR isoforms by the muscle, and interactions with other cells in the local environment.

Animals↗