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Deep proteome profiling of dorsal root ganglia after nerve injury deciphers shared signatures in adolescent and adult male and female mice

ABSTRACT: Our understanding of how sex and age influence pathological pain at the molecular level is still limited. This is of high relevance for pediatric and adolescent patients, as they are known to be particularly vulnerable to long-term consequences of pathological pain. Here, we leveraged deep proteome profiling of mouse dorsal root ganglia (DRG) from the spared nerve injury (SNI)-model of neuropathic pain and investigated adolescent (4-week-old) and adult (12-week-old) male and female mice in parallel. Differential expression and multidimensional analysis enabled us to reveal sex- and age-dependent proteome regulation upon nerve injury. To enhance the translational significance of our findings, we determined shared proteome signatures among tested sex and age groups. By cross-referencing our results with human DRG data evolutionary conserved molecular patterns were identified. These not only bridge the gap between animal models and human biology, but also offer valuable insights for drug discovery efforts benefiting adolescents, women, and men equally. Overall, we provide an innovative resource that allows researchers to gain a more nuanced understanding of nerve injury-induced changes in mouse DRG. Our findings have significant implications for translational research, potentially accelerating discoveries in peripheral nervous system function and pain.

INSTRUMENT(S): timsTOF Pro

ORGANISM(S): Mus Musculus (mouse)

TISSUE(S): Spinal Ganglion

SUBMITTER: Feng Xian

LAB HEAD: Manuela Schmidt

PROVIDER: PXD055816 | Pride | 2024-12-19

REPOSITORIES: Pride

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Project description:Peripheral nerve injury alters the expression of hundreds of proteins in dorsal root ganglia (DRG). Targeting some of these proteins has led to successful treatments for acute pain, but not for sustained postoperative neuropathic pain. The latter may require targeting multiple proteins. Since a single microRNA (miR) can affect the expression of multiple proteins, here, we describe an approach to identify chronic neuropathic pain-relevant miRs. We used two variants of the spared nerve injury (SNI): Sural-SNI and Tibial-SNI and found distinct pain phenotypes between the two. Both models induced strong mechanical allodynia, but only Sural-SNI rats maintained strong mechanical and cold allodynia, as previously reported. In contrast, we found that Tibial-SNI rats recovered from mechanical allodynia and never developed cold allodynia. Since both models involve nerve injury, we increased the probability of identifying differentially regulated miRs that correlated with the quality and magnitude of neuropathic pain and decreased the probability of detecting miRs that are solely involved in neuronal regeneration. We found seven such miRs in L3-L5 DRG. The expression of these miRs increased in Tibial-SNI. These miRs displayed a lower level of expression in Sural-SNI, with four having levels lower than those in sham animals. Bioinformatics analysis of how these miRs could affect the expression of some ion channels supports the view that, following a peripheral nerve injury, the increase of the 7 miRs may contribute to the recovery from neuropathic pain while the decrease of four of them may contribute to the development of chronic neuropathic pain. The approach used resulted in the identification of a small number of potentially neuropathic pain relevant miRs. Additional studies are required to investigate whether manipulating the expression of the identified miRs in primary sensory neurons can prevent or ameliorate chronic neuropathic pain following peripheral nerve injuries. To identify the miRs that were differentially dysregulated between Tibial-SNI and Sural-SNI, we first performed 12 microarrays in a limited number of samples (in four individual DRGs per group: Sham, Tibial-SNI and Sural-SNI; two L3-DRG and two L4-DRG). Then, miRs identified as having differential expression were corroborated with real time qRT-PCR in RNA isolated from individual DRGs (L3, L4 and L5) derived from 4 rats per group (not presented here, but in the manuscript).

			Action	DRS
	GeneGroup_Quant_224Samples.csv	Csv
	Sample_Grouping.xlsx	Xlsx
	mDRG_NeuP_D7-D14.rar	Other
	mDRG_NeuP_D98.rar	Other

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Deep proteome profiling of dorsal root ganglia after nerve injury deciphers shared signatures in adolescent and adult male and female mice

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