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The Journal of Neuroscience, February 2, 2005, 25(5):1103-1112; doi:10.1523/JNEUROSCI.3008-04.2005

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Behavioral/Systems/Cognitive
Nicotine-Induced Antinociception, Rewarding Effects, and Physical Dependence Are Decreased in Mice Lacking the Preproenkephalin Gene

Fernando Berrendero,¹ Victoria Mendizábal,¹ Patricia Robledo,^1,2 Lola Galeote,¹ Andras Bilkei-Gorzo,³ Andreas Zimmer,³ and Rafael Maldonado¹

¹Laboratori de Neurofarmacologia, Facultat de Ciències de la Salut i de la Vida, Universitat Pompeu Fabra, and ²Pharmacology Research Unit, Institut Municipal d'Investigació Mèdica, 08003 Barcelona, Spain, and ³Laboratory of Molecular Neurobiology, Department of Psychiatry, University of Bonn, 53105 Bonn, Germany

It has been shown previously that the endogenous opioid system may be involved in the behavioral effects of nicotine. In the present study, the participation of endogenous enkephalins on nicotine responses has been investigated by using preproenkephalin knock-out mice. Acute nicotine-induced hypolocomotion remained unaffected in these mice. In contrast, antinociception elicited in the tail-immersion and hot-plate tests by acute nicotine administration was reduced in mutant animals. The rewarding properties of nicotine were then investigated using the place-conditioning paradigm. Nicotine induced a conditioned place preference in wild-type animals, but this effect was absent in knock-out mice. Accordingly, in vivo microdialysis studies revealed that the enhancement in dopamine extracellular levels in the nucleus accumbens induced by nicotine was also reduced in preproenkephalin-deficient mice. Finally, the somatic expression of the nicotine withdrawal syndrome precipitated in nicotine-dependent mice by mecamylamine was significantly attenuated in mutant animals. In summary, the present results indicate that endogenous opioid peptides derived from preproenkephalin are involved in the antinociceptive and rewarding properties of nicotine and participate in the expression of physical nicotine dependence.

Key words: nicotine; antinociception; reward; dependence; enkephalin; knock-out mice

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Received March 15, 2004; revised December 14, 2004; accepted December 14, 2004.

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