Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Petsakou, Afroditi; Sapsis, Themistoklis P.; Blau, Justin

doi:10.1016/j.cell.2015.07.010

Cited by 89 publications

(154 citation statements)

References 47 publications

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“…For example, in the moth Manduca sexta , odorant-induced ORN activity appears after the development of the 64 glomeruli (Oland and Tolbert, 1996) and thus, is unlikely to play a role. Therefore, the orco phenotype in ants might be one of the first examples of activity-driven patterning in insects (Petsakou et al, 2015). …”

Section: Discussionmentioning

confidence: 99%

An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

Yan

Opachaloemphan

Mancini

et al. 2017

Cell

201

215

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Summary Ants exhibit cooperative behaviors and advanced forms of sociality that depend on pheromone-mediated communication. Odorant receptor neurons (ORNs) express specific odorant receptors (ORs) encoded by a dramatically expanded gene family in ants. In most eusocial insects, only the queen can transmit genetic information, restricting genetic studies. In contrast, workers in Harpegnathos saltator ants can be converted into gamergates (pseudoqueens) that can found entire colonies. This feature facilitated CRISPR-Cas9 generation of germline mutations in orco, the gene that encodes the obligate co-receptor of all ORs. orco mutations should significantly impact olfaction. We demonstrate striking functions of Orco in odorant perception, reproductive physiology and social behavior plasticity. Surprisingly, unlike in other insects, loss of OR functionality also dramatically impairs development of the antennal lobe where ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.

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Section: Discussionmentioning

confidence: 99%

An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

Yan

Opachaloemphan

Mancini

et al. 2017

Cell

201

215

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“…Toy then activates transcription of Pura , a “plasticity gene” which encodes a Rho1 GEF that increases Rho1 activity and helps retract s-LN v projections to reduce their signaling potency (Fig. 6) (Petsakou et al, 2015). Although many of our experiments used the mammalian Kir2.1 channel to induce hyperpolarization, the Pura transcriptional reporter normally shows a 24hr rhythm in LN v s and can also be induced via an inhibitory neural circuit.…”

Section: Discussionmentioning

confidence: 99%

“…A subset of pacemaker neurons – the 4 small ventral lateral neurons (s-LN v s) in each brain hemisphere – show predictable and intrinsic daily rhythms in their excitability (Cao and Nitabach, 2008) and in the structure of their projections (Cao and Nitabach, 2008; Fernandez et al, 2008). We recently showed that Rho1 activity is rhythmic in s-LN v projections and this is regulated by rhythmic expression of Puratrophin-like ( Pura ), a Rho1 Guanine nucleotide exchange factor (GEF) that increases Rho1 activity (Petsakou et al, 2015). s-LN v plasticity is also regulated by neuronal activity, which normally peaks around dawn (Cao and Nitabach, 2008) when s-LN v projections are maximally expanded.…”

Section: Introductionmentioning

confidence: 99%

A gene expression program activated by neuronal inactivity

Zhu

Ortiz

Mezan

et al. 2019

Preprint

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Long term synaptic plasticity requires transcription in response to changes in neuronal activity. While genes induced by neuronal activity have been extensively studied, genes induced by hyperpolarization are largely unknown. We focused on Pura, a Rho1 GEF whose rhythmic expression drives the daily retraction of the projections of Drosophila LN v circadian pacemaker neurons. We found that Pura transcription is repressed by activity and induced by hyperpolarization in LN v s -the opposite of typical activityregulated genes. Pura is repressed by activity-regulated transcriptional factors including Mef2 and Sr (fly Egr-1) and activated by Toy, a Pax6 transcription factor. toy transcription is also induced by inactivity. Thus toy and Pura represent a class of genes induced by hyperpolarization. Highlights• Hyperpolarization activates transcription of Pura, a plasticity gene • This phenomenon occurs in circadian pacemaker neurons and mushroom body neurons • The Pura enhancer integrates recent neuronal activity to regulate transcription • Hyperpolarization activates transcription of toy (Pax-6), which then activates Pura However, neuronal plasticity also includes reducing neuronal excitability and weakening or losing connections. These aspects of neuronal plasticity are probably important in forgetting memories and also in sleep, in which widespread synaptic downscaling has been proposed to reduce overall connectivity in the brain (de Vivo et al., 2017; Diering et al., 2017). However, relatively few molecular mechanisms have so far been described to explain how neurons decrease their connectivity and the role of gene expression in this phenomenon has been largely ignored. One example of how gene expression can weaken neuronal connections comes fromDrosophila circadian pacemaker neurons, which drive ~24hr rhythms in behavior. A subset of pacemaker neurons -the 4 small ventral lateral neurons (s-LN v s) in each brain hemisphere -show predictable and intrinsic daily rhythms in their excitability (Cao and

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“…We have also combined transgenic RNAi with the inducible GAL80 ts system (McGuire et al, 2003), similar to approaches used in several previous Drosophila studies (Duvall and Taghert, 2012; Zhang et al, 2013; Petsakou et al, 2015). Our behavior and expression data indicate that GAL80 ts is very effective at suppressing da GAL4 activity at 19°C but ineffective at 29°C, although minor decreases in NA expression levels in the 19°C – 19°C condition ( Figure 4A ) could reflect some leakiness of the system.…”

Section: Discussionmentioning

confidence: 99%

The Narrow Abdomen Ion Channel Complex Is Highly Stable and Persists from Development into Adult Stages to Promote Behavioral Rhythmicity

Moose

Haase

Aldrich

et al. 2017

Front. Cell. Neurosci.

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The sodium leak channel NARROW ABDOMEN (NA)/ NALCN is an important component of circadian pacemaker neuronal output. In Drosophila, rhythmic expression of the NA channel regulator Nlf-1 in a subset of adult pacemaker neurons has been proposed to contribute to circadian regulation of channel localization or activity. Here we have restricted expression of Drosophila NA channel subunits or the Nlf-1 regulator to either development or adulthood using the temperature-inducible tubulin-GAL80ts system. Surprisingly, we find that developmental expression of endogenous channel subunits and Nlf-1 is sufficient to promote robust rhythmic behavior in adults. Moreover, we find that channel complex proteins produced during development persist in the Drosophila head with little decay for at least 5–7 days in adults. In contrast, restricting either endogenous or transgenic gene expression to adult stages produces only limited amounts of the functional channel complex. These data indicate that much of the NA channel complex that functions in adult circadian neurons is normally produced during development, and that the channel complex is very stable in most neurons in the Drosophila brain. Based on these findings, we propose that circadian regulation of NA channel function in adult pacemaker neurons is mediated primarily by post-translational mechanisms that are independent of Nlf-1.

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Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Cited by 89 publications

References 47 publications

An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

A gene expression program activated by neuronal inactivity

The Narrow Abdomen Ion Channel Complex Is Highly Stable and Persists from Development into Adult Stages to Promote Behavioral Rhythmicity

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