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The Journal of Neuroscience, August 2, 2006, 26(31):8126-8136; doi:10.1523/JNEUROSCI.0793-06.2006

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Cellular/Molecular
Prolactin Modulates TRPV1 in Female Rat Trigeminal Sensory Neurons

Anibal Diogenes,¹ Amol M. Patwardhan,¹ Nathaniel A. Jeske,² Nikita B. Ruparel,³ Vincent Goffin,⁴ Armen N. Akopian,² and Kenneth M. Hargreaves^1,2

Departments of ¹Pharmacology, ²Endodontics, and ³Cellular Structural Biology, University of Texas Health Science Center at San Antonio, San Antonio, Texas 78229, and ⁴Université Paris Descartes, Faculté de Médecine, Le Site de l’Hôpital Necker, Institut National de la Santé et de la Recherche Médicale, Unité 808, F-75015 Paris, France

Correspondence should be addressed to Dr. Kenneth M. Hargreaves, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78229-3900. Email: hargreaves{at}uthscsa.edu

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--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.

Key words: prolactin; neuropeptide; prolactin receptor; antagonist; estradiol; estrogen; trigeminal; nociceptor; TRPV1; eye-wipe; capsaicin; heat; pain

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Received Feb. 21, 2006; revised June 26, 2006; accepted June 27, 2006.

Correspondence should be addressed to Dr. Kenneth M. Hargreaves, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78229-3900. Email: hargreaves{at}uthscsa.edu

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