Prolactin modulates TRPV1 in female rat trigeminal sensory neurons

Anibal Diogenes, Amol M. Patwardhan, Nathaniel A. Jeske, Nikita B. Ruparel, Vincent Goffin, Armen N. Akopian, Kenneth M. Hargreaves

Research output: Contribution to journalArticle

81 Scopus citations

Abstract

Sex dependency in pain perception is well documented and is thought to be attributable to the effect of reproductive hormones on nociceptive processing. In the present study, we evaluated whether estradiol alters gene transcription in the trigeminal ganglia (TG) of ovariectomized rats (OVX). These experiments demonstrated a dramatic (40-fold) upregulation of prolactin (PRL) expression in TG by 17-β-estradiol (E2). PRL expression was restricted to TG neurons and was highly overlapped with transient potential receptor vanilloid type 1 (TRPV1) (∼90%) in TG. Additionally, PRL is released from neurons during stimulation. Both forms of PRL receptors (PRLRs), short and long, were also present in TG neurons. Moreover, expression of the long PRLRs was under control of estradiol. We next evaluated the novel hypothesis that PRL acts as a neuromodulator of sensory neurons. PRL pretreatment significantly enhanced capsaicin-evoked inward currents, calcium influx, and immunoreactive calcitonin gene-related peptide release from cultured TG neurons. This PRL modulation of capsaicin responses was abolished by withdrawal of E2 from TG cultures. Biochemical analysis demonstrated that PRL increased (>50%) phosphorylation levels of TRPV1 in TG. In a behavioral test, PRL pretreatment significantly potentiated capsaicin-evoked nocifensive behavior in female rats at proestrous and in OVX rats after E2 treatment. The in vivo potentiating effect of PRL on capsaicin responses was also dependent on E2. Collectively, these data demonstrate that PRL is a novel modulator of sensory neurons tightly regulated by E2. These findings are consistent with the hypothesis that PRL could contribute to the development of certain pain disorders, possibly including those modulated by estrogen.

Original languageEnglish (US)
Pages (from-to)8126-8136
Number of pages11
JournalJournal of Neuroscience
Volume26
Issue number31
DOIs
StatePublished - Aug 2 2006
Externally publishedYes

Keywords

  • Antagonist
  • Capsaicin
  • Estradiol
  • Estrogen
  • Eye-wipe
  • Heat
  • Neuropeptide
  • Nociceptor
  • Pain
  • Prolactin
  • Prolactin receptor
  • TRPV1
  • Trigeminal

ASJC Scopus subject areas

  • Neuroscience(all)

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  • Cite this

    Diogenes, A., Patwardhan, A. M., Jeske, N. A., Ruparel, N. B., Goffin, V., Akopian, A. N., & Hargreaves, K. M. (2006). Prolactin modulates TRPV1 in female rat trigeminal sensory neurons. Journal of Neuroscience, 26(31), 8126-8136. https://doi.org/10.1523/JNEUROSCI.0793-06.2006