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The Journal of Neuroscience, January 28, 2004, 24(4):947-955; doi:10.1523/JNEUROSCI.1366-03.2004

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Behavioral/Systems/Cognitive
Estrogen-Induced µ-Opioid Receptor Internalization in the Medial Preoptic Nucleus Is Mediated via Neuropeptide Y-Y₁ Receptor Activation in the Arcuate Nucleus of Female Rats

Richard H. Mills, Richard K. Sohn, and Paul E Micevych

Department of Neurobiology, David Geffen School of Medicine, Laboratory of Neuroendocrinology, Brain Research Institute, University of California, Los Angeles, California 90095

The endogenous peptides -endorphin (-END) and neuropeptide Y (NPY) have been implicated in regulating sexual receptivity. Both -END and NPY systems are activated by estrogen and inhibit female sexual receptivity. The initial estrogen-induced sexual nonreceptivity is correlated with the activation and internalization of µ-opioid receptors (MORs), in the medial preoptic nucleus (MPN). Progesterone reverses the estrogen-induced activation/internalization of MOR and induces the sexual receptive behavior lordosis. To determine whether NPY and endogenous opioids interact, we tested the hypothesis that estrogen-induced MOR activation is mediated through NPY-Y₁ receptor (Y₁R) activation. Retrograde tract tracing demonstrated Y₁Ron -END neurons that projected to the MPN. Sex steroid modulation of MOR in the MPN acts through NPY and the Y₁R. Estradiol administration or intracerebroventricular injection of NPY activated/internalized Y₁R in the arcuate nucleus and MOR in the MPN of ovariectomized (OVX) rats. Moreover, the selective Y₁R agonist [Leu31, Pro34]-Neuropeptide Y (LPNY) internalized MOR in the MPN of OVX rats. The Y₁R antagonist (Cys³¹, Nva³⁴)-Neuropeptide Y (27–36)₂ prevented estrogen-induced Y₁R and MOR activation/internalization. NPY reversed the progesterone blockade of estradiol-induced Y₁R and MOR internalization in the arcuate nucleus and MPN, respectively. Behaviorally, LPNY inhibited estrogen plus progesterone-induced lordosis, and the MOR-selective antagonist D-Phe-Cys-Tyr-d-Trp-Orn-Thr-Pen-Thr amide reversed LPNY-induced inhibition of lordosis. These results suggest that a sequential sex steroid activation of NPY and MOR circuits regulates sexual receptivity.

Key words: internalization; reproduction; hypothalamus; receptors; lordosis; estrogen; progesterone

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Received May 6, 2003; revised November 10, 2003; accepted November 25, 2003.

This article has been cited by other articles:

				P. Dewing, M. I. Boulware, K. Sinchak, A. Christensen, P. G. Mermelstein, and P. Micevych Membrane Estrogen Receptor-{alpha} Interactions with Metabotropic Glutamate Receptor 1a Modulate Female Sexual Receptivity in Rats J. Neurosci., August 29, 2007; 27(35): 9294 - 9300. [Abstract] [Full Text] [PDF]

				Y. R. Smith, C. S. Stohler, T. E. Nichols, J. A. Bueller, R. A. Koeppe, and J.-K. Zubieta Pronociceptive and Antinociceptive Effects of Estradiol through Endogenous Opioid Neurotransmission in Women J. Neurosci., May 24, 2006; 26(21): 5777 - 5785. [Abstract] [Full Text] [PDF]

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