Abstract
Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions. We used RNA sequencing of two-cycle sorted Pirt-positive neurons to identify genes exclusively expressing in L3–L5 DRG, T10-L1 DRG, NG/JG, and TG mouse ganglion neurons. Transcription factor Phox2b and Efcab6 are specifically expressed in NG/JG while Hoxa7 is exclusively present in both T10-L1 and L3–L5 DRG neurons. Cyp2f2, Krt18, and Ptgds, along with pituitary hormone prolactin (Prl), growth hormone (Gh), and proopiomelanocortin (Pomc) encoding genes are almost exclusively in TG neurons. Immunohistochemistry confirmed selective expression of these hormones in TG neurons and dural nerves; and showed GH expression in subsets of TRPV1+ and CGRP+ TG neurons. We next examined GH roles in hypersensitivity in the spinal versus trigeminal systems. Exogenous GH produced mechanical hypersensitivity when injected intrathecally, but not intraplantarly. GH-induced thermal hypersensitivity was not detected in the spinal system. GH dose-dependently generated orofacial and headache-like periorbital mechanical hypersensitivity after administration into masseter muscle and dura, respectively. Periorbital mechanical hypersensitivity was reversed by a GH receptor antagonist, pegvisomant. Overall, pituitary hormone genes are selective for TG versus other ganglia somatotypes; and GH has distinctive functional significance in the trigeminal versus spinal systems.
Highlights
Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions
Using pair comparison and Venn diagram analysis we found Phox2b and Efcab[6] (EF-hand calcium binding domain 6) as Differentially expressing genes (DEG) that were strongly specific to male mouse NG/JG sensory neurons with little-to-no expression in Dorsal root ganglia (DRG) and TG (Fig. 2B; Table 2)
We found Hoxa[7], Hoxa[9], and Hoxa[10] were selectively expressed in L3–L5 DRG compared to NG/JG or TG (Fig. 2C; Table 3)
Summary
Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions. Sensory nerves originating from the cell bodies of these ganglia are classified into nociceptive fibers (unmyelinated C fibers and myelinated Aδ) and low-threshold mechanoreceptors (LTMRs; myelinated Aα and Aβ fibers) Besides their distinct location and innervation pattern, DRG, TG, and NG/JG ganglion sensory neurons each have specialized function with their own respective biochemical and electrical properties. Evidence for these differences has been expanded in recent years with the advent of techniques such as RNA-seq, single-cell. Biomedical Sciences and Translational Sciences, The School of Medicine, UTHSCSA, San Antonio, TX 78229, USA. 4Departments of Microbiology, Immunology and Molecular Genetics, Programs in Integrated Biomedical Sciences and Translational Sciences, The School of Medicine, UTHSCSA, San Antonio, TX 78229, USA. 5Programs in Integrated Biomedical Sciences and Translational Sciences, The School of Medicine, UTHSCSA, San Antonio, TX 78229, USA. 6Greehey Children’s Cancer Research Institute, UTHSCSA, San Antonio, TX 78229, USA. *email: Scientific Reports | (2021) 11:17813
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