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Scaling proprioceptor gene transcription by retrograde NT3 signaling

ABSTRACT: Transcriptional analysis of identified DRG subpopulations. Cell-type specific intrinsic programs instruct neuronal subpopulations before target-derived factors influence later neuronal maturation. Retrograde neurotrophin signaling controls neuronal survival and maturation of dorsal root ganglion (DRG) sensory neurons, but how these potent signaling pathways intersect with transcriptional programs established at earlier developmental stages remains poorly understood. Here we determine the consequences of genetic alternation of NT3 signaling on genome-wide transcription programs in proprioceptors, an important sensory neuron subpopulation involved in motor reflex behavior. We find that the expression of many proprioceptor-enriched genes is dramatically altered by genetic NT3 elimination, independent of survival-related activities. Combinatorial analysis of gene expression profiles with proprioceptors isolated from mice expressing surplus muscular NT3 identifies an anticorrelated gene set with transcriptional levels scaled in opposite directions. Voluntary running experiments in adult mice further demonstrate the maintenance of transcriptional adjustability of genes expressed by DRG neurons, pointing to life-long gene expression plasticity in sensory neurons.

ORGANISM(S): Mus musculus

PROVIDER: GSE38074 | GEO | 2012/08/23

SECONDARY ACCESSION(S): PRJNA167187

REPOSITORIES: GEO

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Scaling proprioceptor gene transcription by retrograde NT3 signaling

Project description:Transcriptional analysis of identified DRG subpopulations. Cell-type specific intrinsic programs instruct neuronal subpopulations before target-derived factors influence later neuronal maturation. Retrograde neurotrophin signaling controls neuronal survival and maturation of dorsal root ganglion (DRG) sensory neurons, but how these potent signaling pathways intersect with transcriptional programs established at earlier developmental stages remains poorly understood. Here we determine the consequences of genetic alternation of NT3 signaling on genome-wide transcription programs in proprioceptors, an important sensory neuron subpopulation involved in motor reflex behavior. We find that the expression of many proprioceptor-enriched genes is dramatically altered by genetic NT3 elimination, independent of survival-related activities. Combinatorial analysis of gene expression profiles with proprioceptors isolated from mice expressing surplus muscular NT3 identifies an anticorrelated gene set with transcriptional levels scaled in opposite directions. Voluntary running experiments in adult mice further demonstrate the maintenance of transcriptional adjustability of genes expressed by DRG neurons, pointing to life-long gene expression plasticity in sensory neurons. We combined a mouse line expressing GFP under the control of the TrkC promoter (BAC transgene approach) with various NT3 signaling mutants in order to identify the transcriptional changes in identified subpopulations of dorsal root ganglia (DRG) neurons. Sorted cells were processed for RNA extraction and hybridization on Affymetrix microarrays. Analysis was performed a postnatal (p) day p0. Subsequent analysis focused on the transcriptional profile of DRG neuron subpopulations at specific lumbar levels. Additional work addressed the transcriptional changes in whole DRG in adult mice with and without physical exercise.

2012-08-23 | E-GEOD-38074 | biostudies-arrayexpress

Molecular distinctions between proprioceptors supplying Tibialis anterior (TA) and Gastrocnemius (GS) muscles [array]

Project description:Muscle-specific populations of proprioceptive sensory neurons form selective connections with spinal motor neurons, implying the existence of molecular distinctions between proprioceptor subpopulations. Here, we compare the gene expression profiles of proprioceptors that supply an antagonistic muscle pair functioning at a single hindlimb joint.

2015-12-02 | GSE70730 | GEO

Molecular distinctions between proprioceptors supplying Tibialis anterior (TA) and Gastrocnemius (GS) muscles [RNA-Seq]

2015-12-02 | GSE71028 | GEO

Origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg

Project description:Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Proprioceptors are diverse: different subtypes detect different features of joint kinematics, such as position, directional movement, and vibration. However, because they are located within complex and dynamic peripheral tissues, the underlying mechanisms of proprioceptor feature selectivity remain poorly understood. Here, we investigate molecular and biomechanical contributions to proprioceptor diversity in the Drosophila leg. Using single-nucleus RNA sequencing, we found that different proprioceptor subtypes express similar complements of mechanosensory and other ion channels. However, anatomical reconstruction of the proprioceptive organ and connected tendons revealed major biomechanical differences between proprioceptor subtypes. We constructed a computational model of the proprioceptors and tendons, which identified a putative biomechanical mechanism for joint angle selectivity. The model also predicted the existence of a goniotopic map of joint angle among position-tuned proprioceptors, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity in Drosophila. More broadly, our discovery of proprioceptive maps in the fly leg reveals common organizational principles between proprioception and other topographically organized sensory systems.

2023-07-03 | GSE236232 | GEO

Transcriptional programs controlled by NGF signaling in developing mouse dorsal root ganglia neurons

Project description:During embryogenesis, nociceptive sensory neurons of the dorsal root ganglia depend intimately on Nerve Growth Factor (NGF) for neuronal survival, maturation and target innervation. NGF is a secreted molecular signal synthesized by neuronal target tissues. In developing nociceptors, NGF engages the receptor tyrosine kinase TrkA to activate a gene transcriptional program involving the regulation of hundreds of transcripts. To identify NGF-dependent genes in developing mouse nociceptors, we have designed and performed two separate microarray screens to compare gene expression profiles of DRG neurons either with or lacking NGF signaling. For the first screen comparing DRGs of BaxM-bM-^HM-^R/M-bM-^HM-^R and NgfM-bM-^HM-^R/M-bM-^HM-^R; BaxM-bM-^HM-^R/M-bM-^HM-^R mice, DRGs were dissected and pooled from E14.5 NgfM-bM-^HM-^R/M-bM-^HM-^R; BaxM-bM-^HM-^R/M-bM-^HM-^R and BaxM-bM-^HM-^R/M-bM-^HM-^R embryos. Total RNA was extracted and directly subjected to microarray analysis. For the second screen comparing mouse DRG explants grown in the presence or absence of NGF, E13.5 mouse DRG explants were cultured for two days with 50 ng/ml of either NGF or NT3. Total RNA was extracted and then subjected to microarray analysis.

2013-11-01 | E-GEOD-25611 | biostudies-arrayexpress

Dicer maintains the identity and function of proprioceptive sensory neurons

Project description:During development neurons achieve a high degree of specialization (Fishell and Heintz, 2013). Over time, while continuously recycling their components and despite transcriptional noise, their own respective properties remain intact. The transcription factors that play a large role in initially establishing neuronal identity can be required for maintaining it (Deneris and Hobert, 2014). Post-transcriptional regulation is also important to differentiation (Bian and Sun, 2011) but its role in maintaining cell identity is less established. To better understand how post-transcriptional regulation might contribute to cell identity, we examined the proprioceptive neurons in the dorsal root ganglion (DRG), a highly specialized sensory class, whose properties are well established and display clear differences when compared to other neurons in the ganglion. By conditionally ablating Dicer in mice, using a parvalbumin (Pvalb) driven cre, we impaired post-transcriptional regulation in the proprioceptive sensory neuron population. KO animals display a progressive form of ataxia at the beginning of the fourth postnatal week that is mirrored by a cell-death within the DRG. Before cell-loss, expression profiling shows a reduction of proprioceptor specific genes and an increased expression of non-proprioceptive genes normally enriched in other ganglion neurons. Furthermore, although central connections of these neurons are intact, the peripheral connections to the muscle are functionally impaired. Post-transcriptional regulation is therefore necessary to retain the transcriptional identity and support functional specialization of the proprioceptive sensory neurons.

2016-12-31 | GSE86019 | GEO

Transcriptome profiles of distinct mechanoreceptive somatosensory neuron subtypes

Project description:The objective of the study was to identify molecules that are selectively expressed in proprioceptive sensory neurons (pSNs) in DRG. To try to achieve this goal, we performed RNAseq on genetically identified and FACS purified cohorts that either contained i) pSNs and rapidly-adapting low threshold mechanoreceptors (RA-LTMRs), iI) pSNs and slowly-adapting (SA)-LTMRs, or RA-LTMRs only. Differential expression analysis between these different sensory neuron cohorts identified multiple proprioceptor enriched transcripts.

2019-03-31 | GSE127161 | GEO

Expression data from mouse proprioceptive sensory neuron subclasses.

Project description:Proprioception relies on two main classes of proprioceptive sensory neurons (pSNs). These neurons innervate two distinct peripheral receptors in muscle, muscle spindles (MSs) or Golgi tendon organs (GTOs), and synapse onto different sets of spinal targets, but the molecular basis of their distinct pSN subtype identity remains unknown. We used microarray analysis to compare gene expression profiles between MS- and GTO- innervating proprioceptors. We generated transgenic mice in which MS and GTO pSNs are labelled with different fluorescent proteins (see de Nooij et al., 2015 for details). We used Fluorescent Activated Cell Sorting (FACS) to isolate the MS and GTO pSN subsets from dissociated DRG from p7-10 transgenic mice. Neurons from multiple FACS experiments were pooled into three samples each for the MS and GTO pSN subset.

2015-01-14 | E-GEOD-64941 | biostudies-arrayexpress

Molecular identity of proprioceptor subtypes innervating different muscle groups in mice

Project description:The precise execution of coordinated movements depends on proprioception, the sense of body position in space. However, the molecular underpinnings of proprioceptive neuron subtype identities are not fully understood. Here we used a single-cell transcriptomic approach to define mouse proprioceptor subtypes according to the identity of the muscle they innervate. We identified and validated molecular signatures associated with proprioceptors innervating back (Tox, Epha3), abdominal (C1ql2), and hindlimb (Gabrg1, Efna5) muscles. We also found that proprioceptor muscle identity precedes acquisition of receptor character and comprise programs controlling wiring specificity. These findings indicate that muscle-type identity is a fundamental aspect of proprioceptor subtype differentiation that is acquired during early development and includes molecular programs involved in the control of muscle target specificity.

2022-10-23 | GSE190605 | GEO

Deregulation of neuronal polarization promotes axonal growth after spinal cord injury

Project description:The developmental maturation of a neuron requires the completion of neuronal polarization preceding the formation of a synapse. Whether neuronal polarization marks the decline in growth competence in the injured mammalian adult nervous system remains elusive. Here we show that gene expression and epigenetic signatures associated with the regenerative growth ability of dorsal root ganglia (DRG) sensory neurons are lost during the transition from a non-polarized to a polarized state. The transcriptional co-factor Cited2 was found to be epigenetically upregulated in immature DRG and following a regenerative injury, but it remained unchanged by a non-regenerative spinal cord injury (SCI). Next, Cited2 was overexpressed in DRG neurons in a model of SCI in mice where it promoted sensory axon growth and reversed the gene expression signatures associated with neuronal maturation. Importantly, Cited2 expression stirred the maturation of DRG neurons towards a non-polarized state. Together, these data suggest that the transition from a non-polarized to a polarized state marks the reversible loss of the regenerative ability of a neuron, thus paving the way to targeted repair strategies relying on neuronal de-maturation.

2024-01-01 | GSE214722 | GEO

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