Immunohistochemical phenotype of sensory neurons associated with sympathetic plexuses in the trigeminal ganglia of adult nerve growth factor transgenic mice.

chronic pain nerve growth factor nociceptors sensory neurons sympathetic plexuses transgenic trigeminal ganglia

Journal

The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041

Informations de publication

Date de publication:
20 Nov 2023
Historique:
pubmed: 21 11 2023
medline: 21 11 2023
entrez: 21 11 2023
Statut: aheadofprint

Résumé

Following peripheral nerve injury, postganglionic sympathetic axons sprout into the affected sensory ganglia and form perineuronal sympathetic plexuses with somata of sensory neurons. This sympathosensory coupling contributes to the onset and persistence of injury-induced chronic pain. We have documented the presence of similar sympathetic plexuses in the trigeminal ganglia of adult mice that ectopically overexpress nerve growth factor (NGF), in the absence of nerve injury. In this study, we sought to further define the phenotype(s) of these trigeminal sensory neurons having sympathetic plexuses in our transgenic mice. Using quantitative immunofluorescence staining analyses, we show that the invading sympathetic axons specifically target sensory somata immunopositive for several biomarkers: NGF high-affinity receptor tyrosine kinase A (trkA), calcitonin gene-related peptide (CGRP), neurofilament heavy chain (NFH), and P2X purinoceptor 3 (P2X3). Based on these phenotypic characteristics, the majority of the sensory somata surrounded by sympathetic plexuses are likely to be NGF-responsive nociceptors (i.e., trkA expressing) that are peptidergic (i.e., CGRP expressing), myelinated (i.e., NFH expressing), and ATP sensitive (i.e., P2X3 expressing). Our data also show that very few sympathetic plexuses surround sensory somata expressing other nociceptive (pain) biomarkers, including substance P and acid-sensing ion channel 3. No sympathetic plexuses are associated with sensory somata that display isolectin B4 binding. Though the cellular mechanisms that trigger the formation of sympathetic plexus (with and without nerve injury) remain unknown, our new observations yield an unexpected specificity with which invading sympathetic axons appear to target a precise subtype of nociceptors. This selectivity likely contributes to pain development and maintenance associated with sympathosensory coupling.

Identifiants

pubmed: 37986234
doi: 10.1002/cne.25563
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Department of Medicine, School of Medicine, Queen's University
Organisme : College of Medicine and College of Science and Health Professions, King Saud bin Abdulaziz University for Health Sciences (Saudi Arabia)

Informations de copyright

© 2023 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.

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Auteurs

Hanin Alsaadi (H)

Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.

Jacob Peller (J)

Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.

Nader Ghasemlou (N)

Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.
Department of Anesthesiology and Perioperative Medicine, School of Medicine, Queen's University, Kingston, Ontario, Canada.
Department of Biomedical and Molecular Sciences, School of Medicine, Queen's University, Kingston, Ontario, Canada.

Michael D Kawaja (MD)

Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.
Department of Biomedical and Molecular Sciences, School of Medicine, Queen's University, Kingston, Ontario, Canada.

Classifications MeSH