Ecdysteroid control of ionic current development inManduca sexta motoneurons

Grünewald, Bernd; Levine, Richard B.

doi:10.1002/(sici)1097-4695(19981105)37:2<211::aid-neu2>3.0.co;2-4

Cited by 31 publications

(24 citation statements)

References 54 publications

(59 reference statements)

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“…Ecdysteroids are indeed able to trigger a cascade of events, involving a complex interplay of nuclear receptors, that allow coordinated and time-delayed expression of numerous proteins, as illustrated by the control of dopa-decarboxylase gene expression (reviewed in Hiruma and Riddiford, 2009), cuticular protein secretion (Charles, 2010) or neuroendocrine cascade regulating ecdysis (reviewed in Žitňan et al, 2007). Importantly, similar long-term effects of ecdysteroids on identified ion channels have been described in insects (see Grünewald and Levine, 1998;Börner et al, 2006;Garrison and Witten, 2010).…”

Section: Mode Of Action Of 20e On Neuronssupporting

confidence: 54%

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

Bacqué-Cazenave

Bouvet

Fossat

et al. 2013

Journal of Experimental Biology

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SUMMARYWe studied the effects of the molting hormone 20-hydroxyecdysone (20E) on leg sensory-motor networks of the red swamp crayfish, Procambarus clarkii. The hormone was injected in isolated crayfish and network activity was analyzed 3days after injection using electrophysiology on an in vitro preparation of the leg locomotor network. This 20E treatment deeply reduced motor activity, by affecting both intrinsic motoneuron (MN) properties and sensory-motor integration. Indeed, we noticed a general decrease in motor nerve tonic activities, principally in depressor and promotor nerves. Moreover, intracellular recordings of depressor MNs confirmed a decrease of MN excitability due to a drop in input resistance. In parallel, sensory inputs originating from a proprioceptor, which codes joint movements controlled by these MNs, were also reduced. The shape of excitatory postsynaptic potentials (PSPs) triggered in MNs by sensory activity of this proprioceptor showed a reduction of polysynaptic components, whereas inhibitory PSPs were suppressed, demonstrating that 20E acted also on interneurons relaying sensory to motor inputs. Consequently, 20E injection modified the whole sensory-motor loop, as demonstrated by the alteration of the resistance reflex amplitude. These locomotor network changes induced by 20E were consistent with the decrease of locomotion observed in a behavioral test. In summary, 20E controls locomotion during crayfish premolt by acting on both MN excitability and sensory-motor integration. Among these cooperative effects, the drop of input resistance of MNs seems to be mostly responsible for the reduction of motor activity.

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Section: Mode Of Action Of 20e On Neuronssupporting

confidence: 54%

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

Bacqué-Cazenave

Bouvet

Fossat

et al. 2013

Journal of Experimental Biology

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“…Consequently, 1 μg/mg is commonly used for Manduca in studies of neuronal structure (Matheson and Levine 1999), motoneuron excitability (Grunewald and Levine 1998), programmed cell death (Zee and Weeks 2001), and myoblast proliferation (Luedeman and Levine 1996) in vitro.…”

Section: Primary Neuron Culturementioning

confidence: 99%

“…For instance, during pupal development of Manduca motoneurons, the amplitude of calcium membrane currents is increased within the first 8 days, whereas the amplitude of potassium membrane currents increases between pupal days 8 and 12 (Duch and Levine 2000). In contrast to the calcium current amplitude, potassium current amplitudes are not affected by ecdysteroid manipulations (Grunewald and Levine 1998). Therefore, membrane currents are affected in a differential fashion by steroids during metamorphosis.…”

Section: Introductionmentioning

confidence: 95%

“…Insect metamorphosis is controlled by ecdysteroids, and manipulations of ecdysteroid titers or their receptors perturb normal development (Weeks 1999;Weeks and Truman 1986;Consoulas et al 2005). Cell culture approaches have demonstrated that ecdysteroids act directly on the isolated somata of Manduca motoneurons to increase neurite outgrowth (Prugh et al 1992;Matheson and Levine 1999) and to mediate changes in the amplitudes of calcium membrane currents (Grunewald and Levine 1998). However, both in vitro and in vivo, these neurons display stage-specific changes in a variety of membrane currents and probably also in their neurotransmitter receptor equipment (Hayashi and Levine 1992;Duch and Levine 2000).…”

Section: Introductionmentioning

confidence: 99%

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A steroid hormone affects sodium channel expression in Manduca central neurons

2006

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Neuronal differentiation is characterized by stereotypical sequences of membrane channel and receptor acquisition. This is regulated by the coordinated interactions of a variety of developmental mechanisms, one of which is the control by steroid hormones. We have used the metamorphosis of the holometabolous insect, Manduca sexta, as a model to study effects of 20-hydroxyecdysone on the maturation of thoracic neuron membrane channel expression. To test for direct hormone action, neurons were dissociated into primary cell culture on the first day of pupal life. In situ hybridization demonstrated that the amount of expression of the acetylcholine receptor alpha subunit, MARA1, was not affected by 20-hydroxyecdysone. Immunocytochemistry with an antibody directed against the SP19 segment of voltage-gated sodium channels revealed no effect of 20-hydroxyecdysone treatment during the first 6 days in culture. SP19 sodium channel protein was evenly distributed along all neurites. In contrast, after 8 days in culture, 20-hydroxyecdysone increased the amount of SP19 protein expression and strongly affected its distribution in differentiating neurons. In the presence of 20-hydroxyecdysone, patches of high densities of SP19 sodium channel protein were found in growth cones close to the base of filopodia. This is a further step toward unraveling the blend of membrane proteins under the control of steroids during the development of the central nervous system of postembryonic Manduca. Our results, taken together with previous studies, indicate that 20-hydroxyecdysone does not affect the expression of potassium membrane current or of the nicotinic acetylcholine receptor but instead regulates the amplitude of the calcium membrane current and the amount and distribution of SP19 sodium channel protein.

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“…Steroid-mediated transcriptional control of ion channel gene expression could alter the electrical properties of larval neurons and muscles to tailor their electrical properties for new adult circuits and behavior. Developmental changes in potassium currents occur in Manduca leg (Hayashi and Levine, 1992;Grüenwald and Levine, 1998), flight motoneurons (Duch et al, 2000;Hayashi and Levine, 1992), antennal lobe neurons (Mercer and Hildebrand, 2002a,b) and glia (Lohr et al, 2001), but the ion channel genes or gene products producing these potassium currents are not known yet.…”

Section: Steroid Hormone Modulation Of Ion Channel Gene Expressionmentioning

confidence: 99%

Calcium-activated potassium channel of the tobacco hornworm,Manduca sexta: molecular characterization and expression analysis

Keyser

Witten

2005

Journal of Experimental Biology

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Large-conductance calciumand voltage-gated potassium channels (BK or Slowpoke) serve as dynamic integrators linking electrical signaling and intracellular activity. These channels can mediate many different Ca 2+ -dependent physiological processes including the regulation of neuronal and neuroendocrine cell excitability and muscle contraction. To gain insights into the function of BK channels in vivo, we isolated a full-length cDNA encoding the alpha subunit of a Slowpoke channel from the tobacco hornworm, Manduca sexta (msslo). Amino acid sequence comparison of the deduced Manduca protein revealed at least 80% identity to the insect Slo channels. The five C-terminal alternative splice regions are conserved, but the cloned cDNA fragments contained some unique combinations of exons E, G and I. Our spatial profile revealed that transcript levels were highest in skeletal muscle when compared with the central nervous system (CNS) and visceral muscle. The temporal profile suggested that msslo expression is regulated developmentally in a tissue-and regional-specific pattern. The levels of msslo transcripts remain relatively constant throughout metamorphosis in the CNS, transiently decline in the heart and are barely detectable in the gut except in adults. A dramatic upregulation of msslo transcript levels occurs in thoracic but not abdominal dorsal longitudinal body wall muscles (DLM), suggesting that the msSlo current plays an important role in the excitation or contractile properties of the phasic flight muscle. Our developmental profile of msslo expression suggests that msSlo currents may contribute to the changes in neural circuits and muscle properties that produce stage-specific functions and behaviors.

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Ecdysteroid control of ionic current development inManduca sexta motoneurons

Cited by 31 publications

References 54 publications

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

A steroid hormone affects sodium channel expression in Manduca central neurons

Calcium-activated potassium channel of the tobacco hornworm,Manduca sexta: molecular characterization and expression analysis

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