Members of the CUGBP Elav‐like family of RNA‐binding proteins are expressed in distinct populations of primary sensory neurons

Author:

Grlickova‐Duzevik Eliza12,Reimonn Thomas M.3,Michael Merilla12,Tian Tina456ORCID,Owyoung Jordan67,McGrath‐Conwell Aidan28,Neufeld Peter28ORCID,Mueth Madison29,Molliver Derek C.12,Ward Patricia Jillian56,Harrison Benjamin J.12ORCID

Affiliation:

1. Biomedical Sciences, College of Osteopathic Medicine University of New England Biddeford Maine USA

2. Center for Excellence in the Neurosciences University of New England Biddeford Maine USA

3. Program in Bioinformatics and Integrative Biology University of Massachusetts Medical School Worcester Massachusetts USA

4. Medical Scientist Training Program Emory University Atlanta Georgia USA

5. Neuroscience Graduate Program Emory University Atlanta Georgia USA

6. Department of Cell Biology Emory University School of Medicine Atlanta Georgia USA

7. Genetics and Molecular Biology Graduate Program Emory University Atlanta Georgia USA

8. College of Arts and Sciences University of New England Biddeford Maine USA

9. Graduate School of Biomedical Science and Engineering University of Maine Orono Maine USA

Abstract

AbstractPrimary sensory dorsal root ganglia (DRG) neurons are diverse, with distinct populations that respond to specific stimuli. Previously, we observed that functionally distinct populations of DRG neurons express mRNA transcript variants with different 3′ untranslated regions (3′UTRs). 3′UTRs harbor binding sites for interaction with RNA‐binding proteins (RBPs) for transporting mRNAs to subcellular domains, modulating transcript stability, and regulating the rate of translation. In the current study, analysis of publicly available single‐cell RNA‐sequencing data generated from adult mice revealed that 17 3′UTR‐binding RBPs were enriched in specific populations of DRG neurons. This included four members of the CUG triplet repeat (CUGBP) Elav‐like family (CELF): CELF2 and CELF4 were enriched in peptidergic, CELF6 in both peptidergic and nonpeptidergic, and CELF3 in tyrosine hydroxylase‐expressing neurons. Immunofluorescence studies confirmed that 60% of CELF4+ neurons are small‐diameter C fibers and 33% medium‐diameter myelinated (likely Aδ) fibers and showed that CELF4 is distributed to peripheral termini. Coexpression analyses using transcriptomic data and immunofluorescence revealed that CELF4 is enriched in nociceptive neurons that express GFRA3, CGRP, and the capsaicin receptor TRPV1. Reanalysis of published transcriptomic data from macaque DRG revealed a highly similar distribution of CELF members, and reanalysis of single‐nucleus RNA‐sequencing data derived from mouse and rat DRG after sciatic injury revealed differential expression of CELFs in specific populations of sensory neurons. We propose that CELF RBPs may regulate the fate of mRNAs in populations of nociceptors, and may play a role in pain and/or neuronal regeneration following nerve injury.

Funder

National Institute of Neurological Disorders and Stroke

National Institute of General Medical Sciences

National Institutes of Health

Publisher

Wiley

Subject

General Neuroscience

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