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Global transcriptome analysis reveals differences between embryonic and adult dorsal root ganglion axonal mRNAs that are implicated in axonal growth and pain

ABSTRACT: Local protein synthesis in sensory neuron axons is necessary for axonal regeneration with the efficiency of regeneration decreasing with age. Because the full repertoire of transcripts in embryonic and adult rat sensory axons is unknown we asked how the pool of mRNAs dynamically changes during ageing. We isolated mRNA from pure axons and growth cones devoid of non-neuronal or cell body contamination. Genome-wide microarray analysis reveals that a previously unappreciated number of transcripts are localised in sensory axons and that this repertoire changes during development toward adulthood. Embryonic sensory axons are enriched in transcripts encoding cytoskeletal-related proteins with a role in axonal outgrowth. Surprisingly, adult axons are highly enriched in mRNAs encoding immune molecules with a role in nociception. To validate our experimental approach we show that Tubulin-beta3 mRNA is present only in embryonic axons where it is locally synthesised. In summary, we show that the population of axonal mRNAs dynamically changes during development, which may partly contribute to the intrinsic capacity of axons at different ages to regenerate after injury and to modulate pain.

ORGANISM(S): Rattus norvegicus

PROVIDER: GSE22638 | GEO | 2010/11/23

SECONDARY ACCESSION(S): PRJNA128107

REPOSITORIES: GEO

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Global transcriptome analysis reveals differences between embryonic and adult dorsal root ganglion axonal mRNAs that are implicated in axonal growth and pain

Project description:Local protein synthesis in sensory neuron axons is necessary for axonal regeneration with the efficiency of regeneration decreasing with age. Because the full repertoire of transcripts in embryonic and adult rat sensory axons is unknown we asked how the pool of mRNAs dynamically changes during ageing. We isolated mRNA from pure axons and growth cones devoid of non-neuronal or cell body contamination. Genome-wide microarray analysis reveals that a previously unappreciated number of transcripts are localised in sensory axons and that this repertoire changes during development toward adulthood. Embryonic sensory axons are enriched in transcripts encoding cytoskeletal-related proteins with a role in axonal outgrowth. Surprisingly, adult axons are highly enriched in mRNAs encoding immune molecules with a role in nociception. To validate our experimental approach we show that Tubulin-beta3 mRNA is present only in embryonic axons where it is locally synthesised. In summary, we show that the population of axonal mRNAs dynamically changes during development, which may partly contribute to the intrinsic capacity of axons at different ages to regenerate after injury and to modulate pain. Pure axonal RNA were extracted from the axons of embryonic and adult dorsal root ganglion neurons, each with 5 biological replicates. The axonal transcriptomes were analysed using Affymetrix Rat Genome 230 2.0 Arrays.

2010-11-23 | E-GEOD-22638 | biostudies-arrayexpress

Axonal mRNA in human embryonic stem cell derived neurons

Project description:The identification of axonal mRNAs in model organisms has led to the discovery of many axonally translated proteins required for axon guidance and injury response. The extent to which these axonal mRNAs are conserved in humans is unknown. Here we report on the axonal transcriptome of glutamatergic neurons derived from human embryonic stem cells (hESC-neurons) grown in axon isolating microfluidic chambers. We identified mRNAs enriched in axons, representing a functionally unique local transcriptome as compared to the whole neuron transcriptome. Further, we found that the enriched functional categories within high confidence axonal transcripts resemble those in the axonal transcriptome of rat cortical neurons. Comparing our list of human axonal transcripts to similar datasets generated from embryonic and adult rat dorsal root ganglia and rat cortical neurons we found 60 mRNAs common to all four neuron types. We found that over half of these genes are associated with neurological phenotypes or diseases in model organisms and human. This data provides an important resource for studying local mRNA translation in human axons and has the potential to reveal both conserved and unique axonal mechanisms across species and neuronal types. We analyzed the axonal and whole hESC-neuron transcriptome in triplicate using the Affymetrix Human Gene 2.0 ST Array platform.

2016-07-29 | E-GEOD-84975 | biostudies-arrayexpress

Axonal mRNA in human embryonic stem cell derived neurons

2016-07-29 | GSE84975 | GEO

Subcellular transcriptome alterations in a cell culture model of spinal muscular atrophy point to widespread defects in axonal growth and presynaptic differentiation

Project description:Neuronal function critically depends on coordinated subcellular distribution of mRNAs. Disturbed mRNA processing and axonal transport has been found in spinal muscular atrophy and could be causative for dysfunction and degeneration of motoneurons. Despite the advances made in characterizing the transport mechanisms of several axonal mRNAs, an unbiased approach to identify the axonal repertoire of mRNAs in healthy and degenerating motoneurons has been lacking. Here we used compartmentalized microfluidic chambers to investigate the somatodendritic and axonal mRNA content of cultured motoneurons by microarray analysis. In axons, transcripts related to protein synthesis and energy production were enriched relative to the somatodendritic compartment. Knockdown of Smn, the protein deficient in spinal muscular atrophy, produced a large number of transcript alterations in both compartments. Transcripts related to immune functions, including MHC class I genes, and with roles in RNA splicing were upregulated in the somatodendritic compartment. On the axonal side, transcripts associated with axon growth and synaptic activity were downregulated. These alterations provide evidence that subcellular localization of transcripts with axonal functions as well as regulation of specific transcripts with nonautonomous functions is disturbed in Smn-deficient motoneurons, most likely contributing to the pathophysiology of spinal muscular atrophy.

2014-12-01 | GSE59506 | GEO

Sub-Cellular Transcriptomics M-bM-^@M-^S Dissection of the mRNA composition in the axonal compartment of sensory neurons

Project description:RNA localization is a regulatory mechanism that is conserved from bacteria to mammals. Yet, little is known about the mechanism and the logic that govern the distribution of RNA transcripts within the cell. Here we present a novel organ culture system, which enables the isolation of RNA specifically from NGF dependent re-growing peripheral axons of mouse embryo sensory neurons. In combination with massive parallel sequencing technology, we determine the sub-cellular localization of most transcripts in the transcriptome. We found that the axon is enriched in mRNAs that encode secreted proteins, transcription factors and the translation machinery. In contrast, the axon was largely depleted from mRNAs encoding transmembrane proteins, a particularly interesting finding, since many of these gene products are specifically expressed in the tip of the axon at the protein level. Comparison of the mitochondrial mRNAs encoded in the nucleus with those encoded in the mitochondria, uncovered completely different localization pattern, with the latter much enriched in the axon fraction. This discovery is intriguing since the protein products encoded by the nuclear and mitochondrial genome form large co-complexes. Finally, focusing on alternative splice variants that are specific to axonal fractions, we find short sequence motifs that are enriched in the axonal transcriptome. Together our findings shed light on the extensive role of RNA localization and its characteristics. For each RNA sample, Spinal Cords\ DRGs were dissected from 40 E13.5 embryos and cultured for 48H. Total RNA was extracted from whole DRG and Peripheral axons. Poly-A enriched. In duplicates, using GAIIx. Read length - 80nt.

2013-10-24 | E-GEOD-51572 | biostudies-arrayexpress

Signaling to Transcription Networks in the Neuronal Retrograde Injury Response

Project description:Retrograde signaling from axon to soma activates intrinsic regeneration mechanisms in lesioned peripheral sensory neurons; however, the links between axonal injury signaling and the cell body response are not well understood. Here, we used phosphoproteomics and microarrays to implicate ~900 phosphoproteins in retrograde injury signaling in rat sciatic nerve axons in vivo and ~4500 transcripts in the in vivo response to injury in the dorsal root ganglia. Computational analyses of these data sets identified ~400 redundant axonal signaling networks connected to 39 transcription factors implicated in the sensory neuron response to axonal injury. Experimental perturbation of individual overrepresented signaling hub proteins, including Abl, AKT, p38, and protein kinase C, affected neurite outgrowth in sensory neurons. Paradoxically, however, combined perturbation of Abl together with other hub proteins had a reduced effect relative to perturbation of individual proteins. Our data indicate that nerve injury responses are controlled by multiple regulatory components, and suggest that network redundancies provide robustness to the injury response Microarrays were run on mRNA extracted from adult rat L4 and L5 DRGs cells after 1,3,8,12,16,18,24, and 28 hours after a sciatic nerve (proximal and distal) lesion.

2010-12-29 | E-GEOD-26350 | biostudies-arrayexpress

Sub-Cellular Transcriptomics – Dissection of the mRNA composition in the axonal compartment of sensory neurons

2013-10-24 | GSE51572 | GEO

Post-transcriptional regulation of adult CNS axonal regeneration by Cpeb1

Project description:Post-transcriptional regulation of gene expression plays important roles in neuron physiology, and likely do so as well in injury response of axons We used microarray to profile expression changes in total and polysome-bound RNA upon spinal cord injury, to elucidate the role of post-transcriptional regulation towards axonal regeneration

2017-10-01 | GSE92657 | GEO

Changes of axonal transcriptomes in response to local Abeta

Project description:We report that local application of Abeta(1-42) for 24h triggers changes in the localized transcriptome, while the transcriptome in cell bodies remains largely unchanged. Axonal and somatic mRNA profiles of rat embryonic hippocampal neurons grown in microfluidic chambers were generated by RNA-Seq in duplicates using an Illumina MiSeq. Axons only were treated for 24 h with soluble oligomeric Abeta(1-42) or vehicle control.

2015-07-14 | E-GEOD-70860 | biostudies-arrayexpress

Transcriptional reprogramming of distinct peripheral sensory neuron subtypes after axonal injury

Project description:Primary somatosensory neurons specialize in transmitting distinct types of sensory information through differences in cell size, myelination, and the expression of various receptors and ion channels, which together define their transcriptional and functional identity. By profiling sensory ganglia at single-cell resolution, we find that the different somatosensory neuronal subtypes undergo a similar transcriptional response to peripheral nerve injury that both promotes axonal regeneration and suppresses cell identity. This transcriptional reprogramming, which is not observed in non-neuronal cells from sensory ganglia, resolves over a similar time course as target reinnervation and is associated with the restoration of original cell identity. Injury-induced transcriptional reprogramming requires ATF3, a transcription factor which is induced rapidly after injury and necessary for axonal regeneration and functional recovery. Our findings suggest that the transcription factors induced early after peripheral sensory neuron injury promote their transcriptional and functional metamorphosis, analogous to their known roles in reprogramming cell fate.

2020-07-22 | GSE154659 | GEO

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