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GABAB Receptor Positive Modulation-Induced Blockade of the Rewarding Properties of Nicotine Is Associated with a Reduction in Nucleus Accumbens ∆Fosb Accumulation

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GABAB Receptor Positive Modulation-Induced Blockade of the Rewarding Properties of Nicotine Is Associated with a Reduction in Nucleus Accumbens ∆Fosb Accumulation JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 JPET FastThis articleForward. has not Published been copyedited on and January formatted. 10,The final2007 version as DOI:10.1124/jpet.106.116228 may differ from this version. JPET #116228 1 GABAB Receptor Positive Modulation-Induced Blockade of the Rewarding Properties of Nicotine is Associated with a Reduction in Nucleus Accumbens ∆FosB Accumulation Cedric Mombereau, Loic Lhuillier, Klemens Kaupmann and John F. Cryan Neuroscience Research, Novartis Institutes for BioMedical Research, Novartis Pharma AG, Basel, Switzerland (CM, LL, KK, JFC) Downloaded from jpet.aspetjournals.org at ASPET Journals on September 25, 2021 Copyright 2007 by the American Society for Pharmacology and Experimental Therapeutics. JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 This article has not been copyedited and formatted. The final version may differ from this version. JPET #116228 2 Running Title: GABAB receptor modulator blocks nicotine-induced changes Corresponding author: John F. Cryan Ph.D School of Pharmacy, Department of Pharmacology & Therapeutics, Cavanagh Pharmacy Building, University College Cork, Cork Ireland Tel: +353 21 4901676 E-Mail: [email protected] Downloaded from Total number of text pages: 18 Number of figures: 6 Number of references: 37 jpet.aspetjournals.org Number of words in Abstract: 250 Number of words in Introduction: 482 Number of words in Discussion: 1,471 Section: Neuropharmacology Abbreviations: GABA, γ –aminobutyric acid; at ASPET Journals on September 25, 2021 JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 This article has not been copyedited and formatted. The final version may differ from this version. JPET #116228 3 ABSTRACT There is an increasing demand for novel non-nicotinic, non-dopaminergic therapeutic approach to nicotine addiction. GABAergic mechanisms have been implicated in drug dependence. Recently, a novel GABAB receptor allosteric positive modulator, GS39783 was characterized. There are no investigations to date on the effects of GABAB receptor positive modulators in animal models of nicotine reinforcement. Conditioned place preference (CPP) paradigms are based upon the principle that animals, like humans, would learn to seek environmental stimuli Downloaded from which have been previously associated with rewarding events. Here we demonstrate that nicotine (0.06 mg/kg s.c.) induced a robust CPP response. Further, GS39783 (30-100 mg/kg. p.o.), during the conditioning phase blocked the rewarding effects of nicotine in the CPP paradigm in rats. jpet.aspetjournals.org However, GS39783 did not significantly alter the CPP effects of nicotine when given only immediately prior to the CPP test. A growing body of evidence suggests that repeated at ASPET Journals on September 25, 2021 administration of drugs of abuse induced long-term molecular changes in brain plasticity, most notably an accumulation of ∆FosB, in the striatal complex, that contribute to the manifestation of dependence. There was a significant accumulation of ∆FosB in the nucleus accumbens, but not dorsal striatum, of rats treated daily for five days with nicotine (0.06mg/kg i.p). GS39783 completely (30-100 mg/kg, po) counteracted these nicotine-induced molecular adaptations when given prior to the CPP acquisition phase but not when administered immediately prior to the test phase. Taken together, the behavioural and molecular changes induced by nicotine occur in concert and are concomitantly amenable to reversal by GABAB receptor positive modulators. JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 This article has not been copyedited and formatted. The final version may differ from this version. JPET #116228 4 Smoking-related illness is a major public health problem in today’s society being the second-leading cause of death in the world (Esson and Leeder, 2004). Therefore, there is great impetus to develop effective therapies that will aid in facilitating smoking cessation. It is largely accepted that nicotine is the active ingredient in tobacco smoke that leads to and maintains tobacco addiction (Goldberg et al., 1989). Therefore, most preclinical research efforts are directed at developing interventions that alter the rewarding components of nicotine. A growing body of evidence suggests that repeated administration of drugs of abuse Downloaded from induce long-term molecular changes in brain plasticity that contribute to the manifestation of dependence (Kelz and Nestler, 2000). Members of the AP-1 family of transcription factors are specifically thought to be involved in the ontogeny of addiction. Indeed, repeated administration jpet.aspetjournals.org of a variety of drugs of abuse, including nicotine induces an accumulation of ∆FosB, a highly stable truncated form of FosB, in the striatal complex (Kelz and Nestler, 2000). Moreover, mice ∆ overexpressing FosB also show enhanced sensitivity to the rewarding effects of cocaine and at ASPET Journals on September 25, 2021 morphine (Kelz and Nestler, 2000). Thus, one can hypothesize that any potential successful therapy for nicotine dependence should attenuate both the rewarding and the molecular changes induced by nicotine. A number of preclinical and clinical studies suggest that activation of GABAB receptor may be a useful strategy for cocaine, opiate and alcohol dependence (Brebner et al., 2002; Cousins et al., 2002). Recently, polymorphisms within the GABAB(2) subunit gene have also been shown to be associated with nicotine dependence in humans (Beuten et al., 2005). Furthermore, GABAB receptor agonists such as baclofen reduce nicotine self-administration in rats (Corrigall, 1999). However, baclofen has many side-effects including sedation, muscle relaxation and hypothermia that could limit its widespread use. Positive modulation of metabotropic receptors is a novel principle for enhancing neurotransmission in a use-dependent fashion. Recently, a novel GABAB receptor allosteric positive modulator, GS39783 was JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 This article has not been copyedited and formatted. The final version may differ from this version. JPET #116228 5 characterized (Urwyler et al., 2003; Cryan et al., 2004). GS39783 increases both the potency and efficacy of endogenous GABA at GABAB receptors without having intrinsic activity (Urwyler et al., 2003; Cryan et al., 2004). Hence, GS39783 lacks many of the behavioural and physiological side-effects of full GABAB receptor agonists (Cryan et al., 2004). Of particular interest, GS39783 reduces the behavioral effects of cocaine (Smith et al., 2004; Slattery et al., 2005; Lhuillier et al., 2006). However, to our knowledge there are no investigations to date on the effects of GS39783 in animal models of nicotine reinforcement. Downloaded from Animals, like humans, learn to seek environmental stimuli which have been previously associated with rewarding events, a process known as conditioned place preference (CPP). Consequently most drugs of abuse including nicotine are effective in supporting CPP, making it jpet.aspetjournals.org a prime test of nicotine reinforcement (Tzschentke, 1998). In the present studies, we investigated the effects of GS39783 on the behavioural (establishment of CPP), and molecular (accumulation ∆ of FosB in the nucleus accumbens) consequences of nicotine exposure. at ASPET Journals on September 25, 2021 JPET Fast Forward. Published on January 10, 2007 as DOI: 10.1124/jpet.106.116228 This article has not been copyedited and formatted. The final version may differ from this version. JPET #116228 6 METHODS Animals Wistar rats, (Charles-River, France) weighing 180-220g at the beginning of the experiments were housed four per cage (55x33x19 cm) in a humidity- and temperature-controlled room under a 12 h light/dark cycle (lights on at 0700). One week prior to the beginning of the experiments, all animals were food-restricted (20g/day) until the end of the study. This was carried out as food restriction has been reported to enhance the rewarding effects of drugs of abuse (Carr 2002) Downloaded from including nicotine (Donny et al. 1998) and the study on which our protocol is based on uses a food restriction regime (Forget et al., 2005). Experiments were subject to institutional review and conducted in accordance with the Veterinary Authority of Basel-Stadt, Switzerland. jpet.aspetjournals.org Conditioned place preference The procedure was carried out essentially as described earlier (Forget et al., 2005). Rats were at ASPET Journals on September 25, 2021 trained and tested in black wooden open fields (76×76×50 cm) located in a dimly lit room (red- light). The floor of each open field was covered with removable quadrants made from wire mesh or rough Plexiglas. These textures were chosen on the basis of previous studies indicating that naive rats exhibited no unconditioned preference for one of them (Forget et al., 2005). The general procedure consisted of two phases: conditioning and testing. Conditioning consisted of alternating four drug-paired conditioning sessions with four vehicle-paired sessions. During drug-paired sessions, nicotine and/or GS39783 were administered (immediately and 30 minutes, respectively) prior to exposure to an open-field covered with one floor texture. Conversely, vehicle paired session consist in pairing vehicle injection with the other floor texture. Initially, half of rats
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