Whole transcriptome expression of trigeminal ganglia compared to dorsal root ganglia in Rattus Norvegicus

Kogelman, Lisette J. A.; Christensen, Rikke; Pedersen, S.; Bertalan, Marcelo; Hansen, Thomas Folkmann; Jansen‐Olesen, Inger; Olesen, Jes

doi:10.1016/j.neuroscience.2017.03.027

Cited by 38 publications

(45 citation statements)

References 45 publications

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“…Advances in next-generation sequencing have allowed the characterization of DRG and TG tissues at the genome-wide level using RNA sequencing (RNA-seq) (Manteniotis et al, 2013;Reynders et al, 2015;Gong et al, 2016;Hu et al, 2016;Kogelman et al, 2017). These studies provide significant insight into genes that are differentially expressed between these tissues, including differences between species (Manteniotis et al, 2013;Flegel et al, 2015;Kogelman et al, 2017). However, these studies lack celltype specificity and fail to capture translational efficiency.…”

Section: Introductionmentioning

confidence: 99%

Differences between Dorsal Root and Trigeminal Ganglion Nociceptors in Mice Revealed by Translational Profiling

Megat¹,

Ray²,

Tavares‐Ferreira³

et al. 2019

J. Neurosci.

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Nociceptors located in the trigeminal ganglion (TG) and DRG are the primary sensors of damaging or potentially damaging stimuli for the head and body, respectively, and are key drivers of chronic pain states. While nociceptors in these two tissues show a high degree of functional similarity, there are important differences in their development lineages, their functional connections to the CNS, and recent genome-wide analyses of gene expression suggest that they possess some unique genomic signatures. Here, we used translating ribosome affinity purification to comprehensively characterize and compare mRNA translation in Scn10a-positive nociceptors in the TG and DRG of male and female mice. This unbiased method independently confirms several findings of differences between TG and DRG nociceptors described in the literature but also suggests preferential utilization of key signaling pathways. Most prominently, we provide evidence that translational efficiency in mechanistic target of rapamycin (mTOR)-related genes is higher in the TG compared with DRG, whereas several genes associated with the negative regulator of mTOR, AMP-activated protein kinase, have higher translational efficiency in DRG nociceptors. Using capsaicin as a sensitizing stimulus, we show that behavioral responses are greater in the TG region and this effect is completely reversible with mTOR inhibition. These findings have implications for the relative capacity of these nociceptors to be sensitized upon injury. Together, our data provide a comprehensive, comparative view of transcriptome and translatome activity in TG and DRG nociceptors that enhances our understanding of nociceptor biology.

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Section: Introductionmentioning

confidence: 99%

Differences between Dorsal Root and Trigeminal Ganglion Nociceptors in Mice Revealed by Translational Profiling

Megat¹,

Ray²,

Tavares‐Ferreira³

et al. 2019

J. Neurosci.

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“…Hox genes are recognized for their key role as regulators of system development and cell fate specification during embryogenesis ( Wellik, 2007 ; Mallo and Alonso, 2013 ; Philippidou and Dasen, 2013 ). Their continued presence in adult DRG is the most striking difference between the two types of ganglia: it can be detected at the level of whole TG and DRG ( Manteniotis et al, 2013 ; Flegel et al, 2015 ; Kogelman et al, 2017 ), and similar anterior–posterior patterns are still discernible in adult CNS ( Hutlet et al, 2016 ). In the brain, the expression of Hox genes after development has been linked to the regulation of key proteins that are involved in synapse formation and plasticity ( Hutlet et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

“…Studies have indeed started to characterize DRG and TG neurons at the molecular level using RNA sequencing (RNA-seq) ( Manteniotis et al, 2013 ; Chiu et al, 2014 ; Perkins et al, 2014 ; Thakur et al, 2014 ; Flegel et al, 2015 ; Reynders et al, 2015 ; Hu et al, 2016 ; Sapio et al, 2016 ; Wu et al, 2016 ; Kogelman et al, 2017 ) enabling in-depth analysis and characterization of their genome-wide transcriptional profiles. To date a few studies have reported approximately 200 differentially expressed genes in both rodents and humans ( Manteniotis et al, 2013 ; Flegel et al, 2015 ; Kogelman et al, 2017 ). Among them were many odorant-binding proteins, ion channels, and G protein-coupled receptors ( Manteniotis et al, 2013 ; Flegel et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

The Molecular Fingerprint of Dorsal Root and Trigeminal Ganglion Neurons

Lopes

Denk

McMahon

2017

Front. Mol. Neurosci.

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The dorsal root ganglia (DRG) and trigeminal ganglia (TG) are clusters of cell bodies of highly specialized sensory neurons which are responsible for relaying information about our environment to the central nervous system. Despite previous efforts to characterize sensory neurons at the molecular level, it is still unknown whether those present in DRG and TG have distinct expression profiles and therefore a unique molecular fingerprint. To address this question, we isolated lumbar DRG and TG neurons using fluorescence-activated cell sorting from Advillin-GFP transgenic mice and performed RNA sequencing. Our transcriptome analyses showed that, despite being overwhelmingly similar, a number of genes are differentially expressed in DRG and TG neurons. Importantly, we identified 24 genes which were uniquely expressed in either ganglia, including an arginine vasopressin receptor and several homeobox genes, giving each population a distinct molecular fingerprint. We compared our findings with published studies to reveal that many genes previously reported to be present in neurons are in fact likely to originate from other cell types in the ganglia. Additionally, our neuron-specific results aligned well with a dataset examining whole human TG and DRG. We propose that the data can both improve our understanding of primary afferent biology and help contribute to the development of drug treatments and gene therapies which seek targets with unique or restricted expression patterns.

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“…Intriguingly, it was revealed that there are trigeminal afferents which project to both the meninges and extracranial tissues (Schueler et al, 2013 ). Both human and rodent data point out that gene expression of TRGs is distinct from DRGs (Manteniotis et al, 2013 ; Flegel et al, 2015 ; Kogelman et al, 2017 ; LaPaglia et al, 2017 ). Yet, there have only been few rodent studies investigating gene expression changes in the TRGs after chronic orofacial inflammation (Okumura et al, 2010 ; Chung et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Alterations in the Trigeminal Ganglia, Nucleus and Peripheral Blood Mononuclear Cells in a Rat Orofacial Pain Model

Aczél

Kun

Szöke

et al. 2018

Front. Mol. Neurosci.

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Orofacial pain and headache disorders are among the most debilitating pain conditions. While the pathophysiological basis of these disorders may be diverse, it is generally accepted that a common mechanism behind the arising pain is the sensitization of extra- and intracranial trigeminal primary afferents. In the present study we investigated gene expression changes in the trigeminal ganglia (TRG), trigeminal nucleus caudalis (TNC) and peripheral blood mononuclear cells (PBMC) evoked by Complete Freund's Adjuvant (CFA)-induced orofacial inflammation in rats, as a model of trigeminal sensitization. Microarray analysis revealed 512 differentially expressed genes between the ipsi- and contralateral TRG samples 7 days after CFA injection. Time-dependent expression changes of G-protein coupled receptor 39 (Gpr39), kisspeptin-1 receptor (Kiss1r), kisspeptin (Kiss1), as well as synaptic plasticity-associated Lkaaear1 (Lkr) and Neurod2 mRNA were described on the basis of qPCR results. The greatest alterations were observed on day 3 ipsilaterally, when orofacial mechanical allodynia reached its maximum. This corresponded well with patterns of neuronal (Fosb), microglia (Iba1), and astrocyte (Gfap) activation markers in both TRG and TNC, and interestingly also in PBMCs. This is the first description of up- and downregulated genes both in primary and secondary sensory neurones of the trigeminovascular system that might play important roles in neuroinflammatory activation mechanisms. We are the first to show transcriptomic alterations in the PBMCs that are similar to the neuronal changes. These results open new perspectives and initiate further investigations in the research of trigeminal pain disorders.

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Whole transcriptome expression of trigeminal ganglia compared to dorsal root ganglia in Rattus Norvegicus

Cited by 38 publications

References 45 publications

Differences between Dorsal Root and Trigeminal Ganglion Nociceptors in Mice Revealed by Translational Profiling

Differences between Dorsal Root and Trigeminal Ganglion Nociceptors in Mice Revealed by Translational Profiling

The Molecular Fingerprint of Dorsal Root and Trigeminal Ganglion Neurons

Transcriptional Alterations in the Trigeminal Ganglia, Nucleus and Peripheral Blood Mononuclear Cells in a Rat Orofacial Pain Model

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