Tooth pulp inflammation increases brain-derived neurotrophic factor expression in rodent trigeminal ganglion neurons

L. Tarsa, E. Bałkowiec-Iskra, F. J. Kratochvil, V. K. Jenkins, A. McLean, A. L. Brown, Julie Smith, John (Craig) Baumgartner, Agnieszka Balkowiec

Research output: Contribution to journalArticle

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Abstract

Nociceptive pathways with first-order neurons located in the trigeminal ganglion (TG) provide sensory innervation to the head, and are responsible for a number of common chronic pain conditions, including migraines, temporomandibular disorders and trigeminal neuralgias. Many of those conditions are associated with inflammation. Yet, the mechanisms of chronic inflammatory pain remain poorly understood. Our previous studies show that the neurotrophin brain-derived neurotrophic factor (BDNF) is expressed by adult rat TG neurons, and released from cultured newborn rat TG neurons by electrical stimulation and calcitonin gene-related peptide (CGRP), a well-established mediator of trigeminal inflammatory pain. These data suggest that BDNF plays a role in activity-dependent plasticity at first-order trigeminal synapses, including functional changes that take place in trigeminal nociceptive pathways during chronic inflammation. The present study was designed to determine the effects of peripheral inflammation, using tooth pulp inflammation as a model, on regulation of BDNF expression in TG neurons of juvenile rats and mice. Cavities were prepared in right-side maxillary first and second molars of 4-week-old animals, and left open to oral microflora. BDNF expression in right TG was compared with contralateral TG of the same animal, and with right TG of sham-operated controls, 7 and 28 days after cavity preparation. Our ELISA data indicate that exposing the tooth pulp for 28 days, with confirmed inflammation, leads to a significant upregulation of BDNF in the TG ipsilateral to the affected teeth. Double-immunohistochemistry with antibodies against BDNF combined with one of nociceptor markers, CGRP or transient receptor potential vanilloid type 1 (TRPV1), revealed that BDNF is significantly upregulated in TRPV1-immunoreactive (IR) neurons in both rats and mice, and CGRP-IR neurons in mice, but not rats. Overall, the inflammation-induced upregulation of BDNF is stronger in mice compared to rats. Thus, mouse TG provides a suitable model to study molecular mechanisms of inflammation-dependent regulation of BDNF expression in vivo.

Original languageEnglish (US)
Pages (from-to)1205-1215
Number of pages11
JournalNeuroscience
Volume167
Issue number4
DOIs
StatePublished - Jun 2010

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Trigeminal Ganglion
Brain-Derived Neurotrophic Factor
Rodentia
Tooth
Inflammation
Neurons
Calcitonin Gene-Related Peptide
Chronic Pain
Up-Regulation
Animal Rights
Temporomandibular Joint Disorders
Nociceptors
Nerve Growth Factors
Migraine Disorders
Synapses
Electric Stimulation
Enzyme-Linked Immunosorbent Assay
Immunohistochemistry
Head
Pain

Keywords

  • CGRP
  • ELISA
  • Mouse
  • Nociceptor
  • Rat
  • TRPV1

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Tooth pulp inflammation increases brain-derived neurotrophic factor expression in rodent trigeminal ganglion neurons. / Tarsa, L.; Bałkowiec-Iskra, E.; Kratochvil, F. J.; Jenkins, V. K.; McLean, A.; Brown, A. L.; Smith, Julie; Baumgartner, John (Craig); Balkowiec, Agnieszka.

In: Neuroscience, Vol. 167, No. 4, 06.2010, p. 1205-1215.

Research output: Contribution to journalArticle

Tarsa, L. ; Bałkowiec-Iskra, E. ; Kratochvil, F. J. ; Jenkins, V. K. ; McLean, A. ; Brown, A. L. ; Smith, Julie ; Baumgartner, John (Craig) ; Balkowiec, Agnieszka. / Tooth pulp inflammation increases brain-derived neurotrophic factor expression in rodent trigeminal ganglion neurons. In: Neuroscience. 2010 ; Vol. 167, No. 4. pp. 1205-1215.
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