Regulation of locomotion and motoneuron trajectory selection and targeting by the Drosophila homolog of Olig family transcription factors

Oyallon, Justine; Apitz, Holger; Miguel-Aliaga, Irene; Timofeev, Katarina; Ferreira, Lauren; Salecker, Iris

doi:10.1016/j.ydbio.2012.06.027

Cited by 25 publications

(31 citation statements)

References 96 publications

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“…This analysis showed transient expression of the transcription factors Olig1 , 2/Oli , Rx/Rax , Hes1/dpn , Hes5/E(spl) , Hey2/Hey , Lhx2/ap , and Vsx2/Vsx2 in larval and pupal, but not adult, CCs (Fig 3A). Oli expression was also specifically detected in PRs, consistent with previous studies reporting fly and vertebrate Oli gene expression in both early neural progenitors and specified neurons [86–89]. Further, we detected Sox100B expression in pupal and adult (but not larval) CCs (Fig 3A, S1 Table), similar to the later onset of expression found for its ortholog Sox9 in vertebrate retinal glia [90,91].…”

Section: Resultssupporting

confidence: 91%

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Multifunctional glial support by Semper cells in the Drosophila retina

et al. 2017

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Glial cells play structural and functional roles central to the formation, activity and integrity of neurons throughout the nervous system. In the retina of vertebrates, the high energetic demand of photoreceptors is sustained in part by Müller glia, an intrinsic, atypical radial glia with features common to many glial subtypes. Accessory and support glial cells also exist in invertebrates, but which cells play this function in the insect retina is largely undefined. Using cell-restricted transcriptome analysis, here we show that the ommatidial cone cells (aka Semper cells) in the Drosophila compound eye are enriched for glial regulators and effectors, including signature characteristics of the vertebrate visual system. In addition, cone cell-targeted gene knockdowns demonstrate that such glia-associated factors are required to support the structural and functional integrity of neighboring photoreceptors. Specifically, we show that distinct support functions (neuronal activity, structural integrity and sustained neurotransmission) can be genetically separated in cone cells by down-regulating transcription factors associated with vertebrate gliogenesis (pros/Prox1, Pax2/5/8, and Oli/Olig1,2, respectively). Further, we find that specific factors critical for glial function in other species are also critical in cone cells to support Drosophila photoreceptor activity. These include ion-transport proteins (Na/K+-ATPase, Eaat1, and Kir4.1-related channels) and metabolic homeostatic factors (dLDH and Glut1). These data define genetically distinct glial signatures in cone/Semper cells that regulate their structural, functional and homeostatic interactions with photoreceptor neurons in the compound eye of Drosophila. In addition to providing a new high-throughput model to study neuron-glia interactions, the fly eye will further help elucidate glial conserved "support networks" between invertebrates and vertebrates.

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Section: Resultssupporting

confidence: 91%

“…elegans [89,92–94], but whose function in Drosophila has thus far only been analyzed in motor neuron development [86]. Applying the same targeted RNAi /ERG strategy as above, we tested two independent RNAi lines for each candidate gene, each pair yielding comparable results (S3A Fig).…”

Section: Resultsmentioning

confidence: 99%

Multifunctional glial support by Semper cells in the Drosophila retina

et al. 2017

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“…We screened this Gal4 collection for expression in single classes of MB extrinsic neurons (MB-ENs), and selected two lines -R12G04-Gal4 and R65G01-Gal4 (Jenett et al, 2012). R12G04-Gal4 is driven by regulatory sequence from the Olig (Oli) transcription factor gene (Jenett et al, 2012;Oyallon et al, 2012), expressing in the MB pedunculus-medial lobe and vertical lobe arborizing neuron 2 (MB-MVP2). R65G01-Gal4 is driven by regulatory sequence from the Leonardo (14-3-3ζ -FlyBase) gene (Broadie et al, 1997), with tightly restricted expression in just two projection neurons (PNs).…”

Section: Two Classes Of Mushroom Body Extrinsic Input and Output Neuronsmentioning

confidence: 99%

Activity-dependent FMRP requirements in development of the neural circuitry of learning and memory

2015

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The activity-dependent refinement of neural circuit connectivity during critical periods of brain development is essential for optimized behavioral performance. We hypothesize that this mechanism is defective in fragile X syndrome (FXS), the leading heritable cause of intellectual disability and autism spectrum disorders. Here, we use optogenetic tools in the Drosophila FXS disease model to test activitydependent dendritogenesis in two extrinsic neurons of the mushroom body (MB) learning and memory brain center: (1) the input projection neuron (PN) innervating Kenyon cells (KCs) in the MB calyx microglomeruli and (2) the output MVP2 neuron innervated by KCs in the MB peduncle. Both input and output neuron classes exhibit distinctive activity-dependent critical period dendritic remodeling. MVP2 arbors expand in Drosophila mutants null for fragile X mental retardation 1 (dfmr1), as well as following channelrhodopsin-driven depolarization during critical period development, but are reduced by halorhodopsin-driven hyperpolarization. Optogenetic manipulation of PNs causes the opposite outcome -reduced dendritic arbors following channelrhodopsin depolarization and expanded arbors following halorhodopsin hyperpolarization during development. Importantly, activity-dependent dendritogenesis in both neuron classes absolutely requires dfmr1 during one developmental window. These results show that dfmr1 acts in a neuron type-specific activity-dependent manner for sculpting dendritic arbors during early-use, critical period development of learning and memory circuitry in the Drosophila brain.

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“…Each pool is molecularly defined by the expression of pool-specific TFs, including a unique combination of Hox TFs (Dasen and Jessell, 2009; Philippidou and Dasen, 2013). In Drosophila embryos, subclassess of MNs are also specified by unique combinations of TFs: evenskipped ( eve ) and grain are expressed in six MNs that target dorsal body wall muscles (Fujioka et al, 2003; Garces and Thor, 2006; Landgraf et al, 1999), and Hb9, Nkx6, Islet, Lim3 and Olig2 are required for ventral-targeting MNs (Broihier et al, 2004; Broihier and Skeath, 2002; Certel and Thor, 2004; Oyallon et al, 2012; Thor et al, 1999; Thor and Thomas, 1997). However, each neuronal subtype defined by these TFs includes multiple morphologically distinct neurons, leaving open the question of how individual neuronal morphologies are specified.…”

Section: Introductionmentioning

confidence: 99%

Specification of Individual Adult Motor Neuron Morphologies by Combinatorial Transcription Factor Codes

Enriquez¹,

Venkatasubramanian²,

Baek³

et al. 2015

Neuron

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Summary How the highly stereotyped morphologies of individual neurons are genetically specified is not well understood. We identify six transcription factors (TFs) expressed in a combinatorial manner in seven post-mitotic adult leg motor neurons (MNs) that are derived from a single neuroblast in Drosophila. Unlike TFs expressed in mitotically active neuroblasts, these TFs do not regulate each other's expression. Removing the activity of a single TF resulted in specific morphological defects, including muscle targeting and dendritic arborization, and in a highly specific walking defect in adult flies. In contrast, when the expression of multiple TFs was modified nearly complete transformations in MN morphologies were generated. These results show that the morphological characteristics of a single neuron are dictated by a combinatorial code of morphology TFs (mTFs). mTFs function at a previously unidentified regulatory tier downstream of factors acting in the NB, but independently of factors that act in terminally differentiated neurons.

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Regulation of locomotion and motoneuron trajectory selection and targeting by the Drosophila homolog of Olig family transcription factors

Cited by 25 publications

References 96 publications

Multifunctional glial support by Semper cells in the Drosophila retina

Multifunctional glial support by Semper cells in the Drosophila retina

Activity-dependent FMRP requirements in development of the neural circuitry of learning and memory

Specification of Individual Adult Motor Neuron Morphologies by Combinatorial Transcription Factor Codes

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