| | The role of neuropeptide FF (NPFF) in the expression of sensitization to hyperlocomotor effect of morphine and ethanolReceived 26 May 2006; accepted 15 September 2006. published online 17 November 2006. Abstract Neuropeptide FF (NPFF) has been characterized as an endogenous anti-opioid peptide because its intraventricular injection (icv) reversed morphine- and stress-induced analgesia, and precipitates withdrawal syndrome in morphine-dependent rats. The role of NPFF in other aspects of drug dependence is unknown. Therefore, the aim of this study was to determine NPFF influence on the expression of sensitization to the morphine-induced hyperlocomotion. As the opioid system plays a role in ethanol effects, the influence of NPFF on the expression of sensitization to hyperlocomotor effect of ethanol was also investigated. Our study indicated that acute administration of NPFF (5, 10, 20 nmol, icv) inhibited the expression of morphine-induced sensitization at doses of 10 (P<0.05) and 20nmol (P<0.01), and also inhibited ethanol-induced sensitization at a dose of 20nmol (P<0.01). Furthermore, NPFF inhibited the acute locomotor effect of morphine (10 and 20nmol) but not that of ethanol. NPFF, given alone, did not change the locomotor activity of mice and did not disturb motor coordination of animals in the rotarod test. In conclusion, our experiments indicated that NPFF attenuated the acute morphine locomotion and the expression of sensitization to locomotion. We anticipate that NPFF may be involved in both of these effects. 1. Introduction  Neuropeptides FF (NPFF), AF (NPAF), and SF (NPSF) are homologous, amidated peptides that were originally identified on the basis of sequence similarity to the molluscan neuropeptide FMRF-amide (Yang et al., 1985, Yang and Martin, 1995). They have been hypothesized to have broad functions in the mammalian central nervous system (CNS), including modulation of pain (Yang et al., 1985, Gouarderes et al., 1993) or opiate functions (Tang et al., 1984, Malin et al., 1990), and also influencing cardiovascular regulation (see Panula et al., 1996), and neuroendocrine function(s) (Majane and Yang, 1990, Majane et al., 1993). One of these sequences, NPFF (FLFQPQRF-NH2), has been characterized as an endogenous anti-opioid peptide (Rothman, 1992, Cesselin, 1995). The evidence that NPFF exhibits anti-opioid properties arises from the facts that: (i) it reverses morphine- and stress-induced analgesia when administered intracerebroventricularly (icv) (Tang et al., 1984, Yang et al., 1985, Kavaliers, 1990); and (ii) the anti-NPFF antibodies increase opiate-induced analgesia (Kavaliers and Yang, 1989). On the other hand, this peptide or its analogs, when administered intrathecally (it), induces: (1) long-lasting analgesia, probably by increasing opioid peptides release in the spinal cord through the functional blockade of presynaptic delta-opioid autoreceptors (Ballet et al., 1999, Mauborgne et al., 2001); and (2) potentiates morphine-induced analgesia (Gouarderes et al., 1993, Roumy and Zajac, 1998). The anti-opioid effects of NPFF suggest that the peptide may be involved in endogenous homeostatic system, which attenuates the effects of morphine. These suggestions are supported by the following observations (1) chronic intra-cerebroventricular NPFF administration downregulates mu-opioid binding sites in rat brain (Rothman et al., 1993), (2) opiate receptor stimulation induces NPFF release (Stinus et al., 1995, Devillers et al., 1995), (3) NPFF-like immunoreactivity level is significantly increased in the brain of morphine-pelleted rats (Stinus et al., 1995) and (4) intraventricular (third ventricle) injection of NPFF precipitates withdrawal syndrome in morphine-dependent rats (Malin et al., 1990). NPFF mediates its pharmacological effects by interacting with G-protein-coupled receptors, NPFF1 and NPFF2, (human and rat) (Bonini et al., 2000, Kotani et al., 2001). This peptide does not bind to opioid receptors and, conversely, opioids have no measurable affinity towards NPFF receptors (Allard et al., 1989, Raffa et al., 1994). However, many studies suggest that NPFF mechanisms are functionally coupled to the opioid system (see Panula et al., 1999). The receptors for NPFF are widely expressed in CNS, predominantly in spinal cord and also in the brain regions regulating emotional functions (fear, anxiety, reward) (Liu et al., 2001, Cador et al., 2002). Drug dependence is a chronically relapsing disorder that is characterized by a compulsion to seek and take a drug, and by withdrawal syndromes after abruption of drug taking. Drug reward and phenomenon of sensitization play a crucial role in the development of drug dependence. It has been proposed that sensitization exhibits an important function in the ethiology and maintenance of drug seeking behavior as well as in relapse to this behavior after a period of drug abstinence (Robinson and Berridge, 1993, Stewart and Badiani, 1993). The enhancement of behavioral response to repeated drug administration is typically referred to as behavioral sensitization. Several studies have shown that behavioral sensitization can result from the repeated administration of mu-opioid agonists, such as morphine (Babbini and Davis, 1972, Kalivas and Duffy, 1987), psychomotor stimulants, such as amphetamine (Segal and Mandell, 1974), or cocaine (Segal and Kuczenski, 1992), as well as from the repeated administration of ethanol (Lessov and Phillips, 1998). Drug-induced sensitization develops to the effects of these drugs on locomotor activity (Babbini and Davis, 1972, Robinson and Becker, 1986), but also to their effects on behavioral measures of drug reward, such as self-administration (Piazza et al., 1990), conditioned place preference (Shippenberg et al., 1996), and intracranial self-stimulation (Kokkinnidis and Zacharo, 1980). The aim of the present study was to investigate whether NPFF affects the acute hyperlocomotor effect of morphine and ethanol, and influences the expression of morphine- and ethanol-induced sensitization to their hyperlocomotor effects. 2. Materials and methods All experiments were performed in agreement with ethical regulations and were approved by the Local Ethics Committee. Male Swiss mice (20–25g) were purchased from a local distributor (HZL, Warszawa, Poland) and housed in groups of five, with standard food and free access to water. Animals were maintained in a 12:12h light:dark cycle (light on at 08:00) in an air-conditioned room. After 1week of adaptation and handling, the animals were divided into groups (8–10animals/group) and prepared for the tests. 2.3. Sensitization to morphine Development of sensitization to the hyperlocomotor effect of morphine was based on the method described by Kuribara, 1995, Kuribara, 1997 with minor modification. Mice were divided into two groups, one of which received morphine at the dose of 10mg/kg subcutaneously (sc). Control group received the appropriate volume of saline, five times at 3-day intervals. Locomotor activity was measured in the locomotor activity boxes (round Plexiglas cages, 30cm in diameter, Multiserv, Lublin, Poland) for 60min immediately after each administration. Seven days after the fifth pretreatment with morphine (day 20 of the experiment), the mice previously treated with morphine received the challenge dose of morphine (10mg/kg) and the expression of sensitization to locomotor activity was measured for 60min. To investigate the influence of the peptide on the expression of morphine-induced sensitization, NPFF at the doses of 5, 10 and 20nmol, icv, was given only on day 20 of the experiment, 2min before the challenge dose of morphine. In the separate experiments, the injection of NPFF (5, 10 and 20nmol, icv) on spontaneous locomotor activity of mice was measured. 2.4. Sensitization to ethanol Development of sensitization to the hyperlocomotor effect of ethanol was based on the method described by Lessov and Phillips (1998), with minor modification (Kotlinska et al., 2006). Mice received four intraperitoneal (ip) ethanol injections (on the 1st, 4th, 7th and 10th day), at a dose of 2.4g/kg. The control mice received saline. Four days after the last treatment with ethanol (day 15 of the experiment), mice previously treated with ethanol received the challenge dose of ethanol (2.4g/kg, ip), and the expression of sensitization to locomotor activity was measured for 30min. To investigate the influence of NPFF on the expression of ethanol-induced sensitization, mice received a single injection of the peptide at doses of 5, 10 and 20nmol, 2 min before the challenge dose of ethanol, and then locomotor activity was measured for 30min. 3. Results 3.2. Influence of NPFF given alone, on the locomotor activity of naive mice and the acute morphine- and ethanol-induced hyperlocomotion The statistical analysis revealed that NPFF, given alone at the doses of 5 and 20nmol, did not change the locomotor activity of mice [F(2,23)=1.663; P<0.05] (Fig. 1b). Acute administration of morphine (P<0.01) at the dose of 10mg/kg, ip, or ethanol (P<0.05) at the dose of 2.4g/kg, ip, induced hyperlocomotor effect in mice. NPFF administered at the dose of 5, 10 and 20nmol, icv, 2min before morphine (Fig. 2a) or ethanol (Fig. 2b) decreased the hyperlocomotor effect of morphine at the dose of 10nmol (P<0.05) and 20nmol (P<0.01). NPFF alone did not influence the effect of ethanol. 3.3. Influence of NPFF on the expression of sensitization to hyperlocomotor effect of morphine As shown by the analysis of variance, the locomotor response of mice to morphine and NPFF differed between the groups [F(5,55)=4.5; P<0.01]. The challenge dose of morphine (10mg/kg) induced a significant increase of locomotor activity in mice, in comparison to acute morphine administration (10mg/kg, P<0.01), and to saline group (P<0.001). The acute administration of NPFF at the doses of 5, 10 and 20nmol, icv, 2min before the challenge dose of morphine (10mg/kg), decreased the expression of morphine-induced sensitization. NPFF given at the smallest dose of 5nmol attenuated the morphine sensitization, but the result was not statistically significant. However, higher doses of 10nmol (P<0.05) and 20nmol (P<0.01) significantly decreased the hyperlocomotion induced by challenge dose of morphine. NPFF given at the dose of 5 and 20nmol to saline-treated mice did not change the locomotor activity of animals (Fig. 3). 4. Discussion Our study indicated that the icv injection of NPFF decreased the expression of morphine- and ethanol-induced sensitization to their hyperlocomotor effects. NPFF given alone does not change locomotor activity of naive animals and does not affect motor coordination of mice in rotarod test. However, the peptide inhibited the acute hyperlocomotor effect of morphine but not of ethanol. The hyperlocomotor effect of acute and repeated morphine treatments is mediated by activation of the mesolimbic dopamine system (Joyce and Iversen, 1979, Vezina et al., 1987, Spanagel and Shippenberg, 1993). There is a good evidence that the ventral tegmental area (VTA), the cell body region of the mesolimbic dopamine system, is a critical locus for morphine-induced behavioral sensitization (Vezina et al., 1987, Kalivas and Duffy, 1987), and VTA and nucleus accumbens (NAcc) are dominant brain structures involved in drug-induced reward/reinforcement (Wise and Bozarth, 1987, Berridge and Robinson, 1998). Morphine evokes its rewarding actions in the VTA. Mu-opioid agonists disinhibit the firing of dopaminergic neurons in this region by inhibiting GABAergic interneurons, leading to an increase of dopamine release in the NAcc. An injection of opiates or opioid peptides into the VTA induces behavioral activation reversed either by naloxone or intra-accumbens injection of dopamine receptor antagonists, or by specific lesions of mesolimbic dopamine neurons (Cador et al., 2002). It has been reported that NPFF, injected into the VTA, acts as an anti-opioid peptide because (1) it reduces the locomotor activity triggered by exposure to novelty, (2) decreases dose-dependently the potentiation of novelty-induced locomotor response produced by VTA injection of thiorphan, an inhibitor of enkephalin degradation (Cador et al., 2002) and (3) given into VTA abolishes hyperactivity induced by intra-VTA injection of morphine (Marco et al., 1995). The presence of both NPFF-like immunoreactive material and NPFF binding sites within the VTA (Allard et al., 1992, Marco et al., 1995) suggests that NPFF may be a good candidate involved in regulation of mesocorticolimbic system, directly or indirectly, at VTA level. Our results and others (Cador et al., 2002, Marchand et al., 2006, Marco et al., 1995) indicate that injection of NPFF receptor agonists have minor impact on the locomotor activity of mouse per se, but can decrease the locomotion induced by morphine or stressful conditions. Therefore, our results support the hypothesis about anti-opioid potency of this peptide. Furthermore, our data show that NPFF inhibited the expression of sensitization to hyperlocomotor effect of morphine and of ethanol. It is well known that endogenous opioids play a key role in ethanol drinking (Ng et al., 1996) and in the rewarding properties of ethanol (Herz, 1997). There is much information on the direct or indirect effects of ethanol on the binding properties of opioid receptors, as well as on modulation of opioid peptides biosynthesis and secretion (Herz, 1997). Because the involvement of opioid system in ethanol effects seems to be rather complex and depends also on the interaction with other neurotransmitters, it is possible that opioid system plays a more dominant role in ethanol sensitization than in the acute effect of ethanol. Therefore, NPFF, as an anti-opiod compound, attenuated the chronic effect (senstitization) but not acute hyperlocomotor effect of ethanol in our study. On the other hand, the presence of both NPFF-like immunoreactive material and NPFF binding sites in the mesolimbic structures (Panula et al., 1996, Marco et al., 1995, Allard et al., 1992) may suggest an involvement of NPFF in drug addiction processes (Nestler and Aghajanian, 1997). The destruction of VTA perikarya with ibotenic acid induced a reduction of NPFF receptors in the VTA, while their density was not statistically modified following specific 6-hydroxydopamine lesion of dopamine neurons (Marco et al., 1995). These results exclude the hypothesis that NPFF neurons can directly modulate mesolimbic dopaminergic system, but the peptide may act indirectly through the modulation of the activity of VTA inputs and/or intrinsic VTA non-dopaminergic neurons (Cador et al., 2002). Behavioral sensitization to hyperlocomotor effects of drugs involves changes in many neurotransmitters, such as 5-HT, GABA or excitatory amino acids that interact with the mesolimbic dopaminergic system (Kalivas and Stewart, 1991, Wolf and Jeziorski, 1993). The effect of NPFF injection on monoamines metabolism was examined only in a few studies. Attila et al. (1995) indicated that acute co-administration of NPFF and morphine did not decrease, (as we could predict) but increased dopamine and 5-HT levels in limbic areas. In other study, NPFF potentiated amphetamine-induced sensitization and elevated the levels of glutamate and GABA in the medial prefrontal cortex (mPFC) in amphetamine-sensitized rats, but not in control rats (Chen et al., 1999). It is known that glutamatergic neurons from mPFC innervate the NAcc (Walaas, 1981) and take part in sensitization procesess because systemic injections of glutamate antagonists prevented the acquisition or expression of sensitization to morphine (Del Rosario et al., 2002), amphetamine (Wolf et al., 1995) or ethanol (Kotlinska et al., 2006). Additionally, dynorphin, which is also suggested to play a role as an anti-opioid peptide, and it is released as a consequence of opioid receptor stimulation, evokes glutamate release at the spinal level, thus suggesting that this peptide is involved in the central pain sensitization process induced by opioids (Gardell et al., 2002, Koetzner et al., 2004). Recent study of Simonin et al. (2006) reports that antagonist of both types the NPFF receptor (NPFF1 and NPFF2), prevents pain sensitization induced by daily heroin administration. This finding is in contrast to our data that endogenous agonist of NPFF receptors attenuated the expression of sensitization to hyperlocomotor effect of morphine and ethanol. However, recent study presented by Chen et al. (2006) indicate that the agonist of NPFF1 receptor, PFR(Tic)amide, blocked behavioral sensitization to amphetamine-induced locomotion and these results are not in agreement with those published earlier by the same group (Chen et al., 1999), and describing potentiation of the amphetamine-induced sensitization by NPFF. Furthermore, studies of Marchand et al. (2006) indicated that 1DMe, an agonist of NPFF2 receptor, suppressed the rewarding effects of morphine in the conditioned place preference paradigm. These data show that NPFF receptors may be involved in behavioral sensitization induced not only by opioids but also by psychostimulants. Further studies are necessary to reveal the role of particular agonists and antagonists/or type of NPFF receptor (NPFF1 and/or NPFF2) in inhibition of sensitization. In conclusion, our experiments indicate that NPFF attenuated the acute morphine locomotion and the expression of sensitization to locomotion induced by morphine and ethanol. Our study supports the hypothesis of the existence of a strong inhibitory functional interactions between opioids and NPFF. Acknowledgements This work was supported by the Polish Committee for Scientific research (KBN 3P04B 02024), and by the International Centre for Genetic Engineering and Biotechnology, Trieste (grant ICGEB CRP/POL-05/02). References Allard et al., 1989. 1.Allard M, Geoffre S, Legendre P, Vincent JD, Simonnet G. Characterization of rat spinal cord receptors to FLFQPQRF amide, a mammalian morphine modulating peptide: a binding study. Brain Res. 1989;500:169–176. MEDLINE |
CrossRef
Allard et al., 1992. 2.Allard M, Zajac JM, Simonnet G. Autoradiographic distribution of receptors to FLFQPQRF amide, a morphine-modulating peptide, in rat central nervous system. Neuroscience. 1992;49:101–116. MEDLINE |
CrossRef
Attila et al., 1995. 3.Attila M, Kurkijarvi U, Kivipelto L, Panula P, Ahtee L. The antiopioid peptide, neuropeptide FF, enhances the effects of acute morphine on the cerebral monoamines in rats. Pharmacol. Res. 1995;32:293–298. MEDLINE |
CrossRef
Babbini and Davis, 1972. 4.Babbini M, Davis WM. Time–dose relationships for locomotor activity effects of morphine after acute or repeated treatment. Br. J. Pharmacol. 1972;46:213–224. MEDLINE Ballet et al., 1999. 5.Ballet S, Mauborgne A, Gouarderes C, Bourgoin AS, Hamon M, Zajac J-M, et al. The neuropeptide FF analogue, 1DME, enhances in vivo met-enkephalin release from the rat spinal cord. Neuropharmacology. 1999;38:1317–1324. MEDLINE |
CrossRef
Berridge and Robinson, 1998. 6.Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res. Rev. 1998;28:309–369. MEDLINE |
CrossRef
Bonini et al., 2000. 7.Bonini JA, Jones KA, Adham N, Forray C, Artymyshyn R, Durkin MM, et al. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J. Biol. Chem. 2000;275:39324–39331. MEDLINE |
CrossRef
Cador et al., 2002. 8.Cador M, Marco N, Stinus L, Simonnet G. Interaction between neuropeptide FF and opioids in the ventral tegmental area in the behavioral response to novelty. Neuroscience. 2002;110:309–318. MEDLINE |
CrossRef
Cesselin, 1995. 9.Cesselin F. Opioid and anti-opioid pepides. Fundam. Clin. Pharmacol. 1995;9:409–443. MEDLINE |
CrossRef
Chen et al., 1999. 10.Chen JC, Li JY, Liang KW, Huang YK. Neuropeptide FF potentiates the behavioral sensitization to amphetamine and alters the levels of neurotransmitters in the medial prefrontal cortex. Brain Res. 1999;816:220–224. MEDLINE |
CrossRef
Chen et al., 2006. 11.Chen JC, Lee W-H, Chen P-C, Tseng C-P, Huang EY-K. Rat NPFF1 receptor-mediated signaling: functional comparison of neuropeptide FF (NPFF), FMRFamide and PFR(Tic)amide. Peptides. 2006;27:1005–1014. MEDLINE |
CrossRef
Del Rosario et al., 2002. 12.Del Rosario CN, Pacchioni AM, Cancela LM. Influence of acute or repeated restraint stress on morphine-induced locomotion: involvement of dopamine, opioid and glutamate receptors. Behav. Brain Res. 2002;134:229–238. MEDLINE |
CrossRef
Devillers et al., 1995. 13.Devillers JP, Boisserie F, Laulin JP, Larcher A, Simonnet G. Simultaneous activation of spinal antiopioid system (neuropeptide FF) and pain facilitatory circuitry by stimulation of opioid receptors in rats. Brain Res. 1995;700:173–181. MEDLINE |
CrossRef
Gardell et al., 2002. 14.Gardell LR, Wang R, Burgess SE, Ossipov MH, Vanderah TW, Malan TP, et al. Sustained morphine exposure induces a spinal dynorphin-dependent enhancement of excitatory transmitter release from primary afferent fibers. J. Neurosci. 2002;22:6747–6755. Gouarderes et al., 1993. 15.Gouarderes C, Sutek M, Zajac J-M, Jhamandas K. Antinociceptive effects of intrathecall administerd F8Famide and FMR-Famide in the rat. Eur. J. Pharmacol. 1993;237:73–81. MEDLINE |
CrossRef
Herz, 1997. 16.Herz A. Endogenous opioid system and alcohol addiction. Psychopharmacology. 1997;129:99–111. MEDLINE |
CrossRef
Joyce and Iversen, 1979. 17.Joyce EM, Iversen SD. The effect of morphine applied locally to mesencephalic dopamine cell bodies on spontaneous motor activity in the rat. Neurosci. Lett. 1979;14:207–212. MEDLINE |
CrossRef
Kalivas and Duffy, 1987. 18.Kalivas PW, Duffy P. Sensitization to repeated morphine injection in the rat: possible involvement of A10 dopamine neurons. J. Pharmacol. Exp. Ther. 1987;241:204–212. MEDLINE Kalivas and Stewart, 1991. 19.Kalivas PW, Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Rev. 1991;16:223–244. MEDLINE |
CrossRef
Kavaliers, 1990. 20.Kavaliers M. Inhibitory influences of mammalian FMRFamide (Phe-Met-Arg-Phe-amide)-related peptides on nociception and morphine- and stress-induced analgesia in mice. Neurosci. Lett. 1990;115:307–312. MEDLINE |
CrossRef
Kavaliers and Yang, 1989. 21.Kavaliers M, Yang H-Y. IgG from antiserum against endogenous mammalian FMRF-NH2-related peptides augments morphine- and stress-induced analgesia in mice. Peptides. 1989;10:741–745. MEDLINE |
CrossRef
Koetzner et al., 2004. 22.Koetzner L, Hua XY, Lai J, Porreca F, Yaksh T. Nonopioid actions of intrathecal dynorphin evoke spinal excitatory amino acid and prostaglandin E2 release mediated by cyclooxygenase-1 and -2. J. Neurosci. 2004;24:1451–1458.
CrossRef
Kokkinnidis and Zacharo, 1980. 23.Kokkinnidis L, Zacharo RM. Enhanced self-stimulation responding from the substantia nigra after chronic amphetamine treatment: a role for conditioning factors. Pharmacol. Biochem. Behav. 1980;12:543–547. MEDLINE |
CrossRef
Kotani et al., 2001. 24.Kotani M, Mollereau C, Detheux M, Le Poul E, Brezillon S, Vakili J, et al. Functional characterization of a human receptor for neuropeptide FF and related peptides. Br. J. Pharmacol. 2001;133:138–144. MEDLINE |
CrossRef
Kotlinska et al., 2006. 25.Kotlinska J, Bochenski M, Danysz W. N-methyl-d-aspartate and group I metabotropic glutamate receptors are involved in the expression of ethanol-induced sensitization in mice. Behav Pharmacol. 2006;17:1–8. MEDLINE |
CrossRef
Kuribara, 1995. 26.Kuribara H. Modification of morphine sensitization by opioid and dopamine receptor antagonists: evaluation by studying ambulation in mice. Eur. J. Pharmacol. 1995;275:251–258. MEDLINE |
CrossRef
Kuribara, 1997. 27.Kuribara H. Induction of sensitization to hyperactivity caused by morphine in mice: effects of post-drug environments. Pharmacol. Biochem. Behav. 1997;57:341–346. MEDLINE |
CrossRef
Laursen and Belknap, 1986. 28.Laursen SE, Belknap JK. Intracerebroventricular injections in mice. Some methodological refinements. J. Pharmacol. Meth. 1986;16:355–357. Lessov and Phillips, 1998. 29.Lessov CN, Phillips TJ. Duration of sensitization to the locomotor stimulant effects of ethanol in mice. Psychopharmacology. 1998;135:374–382. MEDLINE |
CrossRef
Liu et al., 2001. 30.Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, et al. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J. Biol. Chem. 2001;276:36961–36969. MEDLINE |
CrossRef
Majane and Yang, 1990. 31.Majanem EA, Yang HY. FMRF-NH2-like peptide is deficient in the pituitary gland of the Brattleboro rat. Peptides. 1990;11:345–349. MEDLINE |
CrossRef
Majane et al., 1993. 32.Majane EA, Zhu J, Aarnisalo AA, Panula P, Yang HY. Origin of neurohypophyseal neuropeptide-FF (FLFQPQRF-NH2). Endocrinoogy. 1993;133:1578–1584. Malin et al., 1990. 33.Malin DH, Lake JR, Fowler DE, Hammond MV, Brown SL, Leyva JE, et al. FMRF-NH2-like mammalian peptide precipitates opiate-withdrawal syndrome in the rat. Peptides. 1990;11:277–280. MEDLINE |
CrossRef
Marchand et al., 2006. 34.Marchand S, Betourne A, Marty V, Daumas S, Halley H, Lassalle JM, et al. A neuropeptide FF agonist blocks the acquisition of conditioned place preference to morphine in C57Bl/6J mice. Peptides. 2006;27:964–972. MEDLINE |
CrossRef
Marco et al., 1995. 35.Marco N, Stinus L, Allard M, Le Moal M, Simonnet G. Neuropeptide FLFQRFamide receptors within the ventral mesencephalon and dopaminergic terminal areas: localization and functional antiopioid involvement. Neuroscience. 1995;64:1035–1044. MEDLINE |
CrossRef
Mauborgne et al., 2001. 36.Mauborgne A, Bourgoin S, Polienor H, Roumy M, Simonnet G, Zajac JM, et al. The neuropeptide FF analogue, 1DMe, acts as a functional opioid autoreceptor antagonist in the rat spinal cord. Eur. J. Pharmacol. 2001;430:273–276. MEDLINE |
CrossRef
Nestler and Aghajanian, 1997. 37.Nestler EJ, Aghajanian GK. Molecular and cellular basis of addiction. Science. 1997;278:58–63. MEDLINE |
CrossRef
Ng et al., 1996. 38.Ng GY, O’Dowd BF, George SR. Genotypic differences in mesolimbic enkephalin gene expression in DBA/2J and C57BL/6J inbred mice. Eur. J. Pharmacol. 1996;311:45–52. MEDLINE |
CrossRef
Panula et al., 1996. 39.Panula P, Aarnisalo AA, Wasowicz K. Neuropeptide FF, a mammalian neuropeptide with multiple functions. Prog. Neurobiol. 1996;48:461–487. Panula et al., 1999. 40.Panula P, Kalso E, Nieminen M, Kontinen VK, Brandt A, Pertovaara A. Neuropeptide FF and modulation of pain. Brain Res. 1999;848:191–196. MEDLINE |
CrossRef
Piazza et al., 1990. 41.Piazza PV, Deminiere JM, le Moal M, Simon H. Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res. 1990;514:22–26. MEDLINE |
CrossRef
Raffa et al., 1994. 42.Raffa RB, Kim A, Rice KC, de Costa BR, Codd EE, Rothman RB. Low affinity of FMRFamide and four FaRPs (FMRFamide-related peptides), including the mammalian-derived FaRPs F-8- amide (NPFF) and A-18-Famide, for opioid mu, delta, kappa 1, kappa 2a, or kappa 2b receptors. Peptides. 1994;15:401–404. MEDLINE |
CrossRef
Robinson and Becker, 1986. 43.Robinson TE, Becker JB. Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res. Rev. 1986;396:157–198. Robinson and Berridge, 1993. 44.Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 1993;18:247–291. MEDLINE |
CrossRef
Rothman, 1992. 45.Rothman RB. review of the role of anti-opioid peptides in morphine tolerance and dependence. Synapse. 1992;12:129–138. MEDLINE |
CrossRef
Rothman et al., 1993. 46.Rothman RB, Brady LS, Xu H, Long JB. Chronic intraventricular infusion of the anti-opiod peptide, Phe-Leu-Phe-Gln-Pro-Gln-Arg-Phe-NH2 (NPFF), downregulates mu opioid binding sites in rat brain. Peptides. 1993;14:1271–1277. MEDLINE |
CrossRef
Roumy and Zajac, 1998. 47.Roumy M, Zajac JM. Neuropeptide FF, pain and analgesia. Eur. J. Pharmacol. 1998;345:1–11. MEDLINE |
CrossRef
Segal and Kuczenski, 1992. 48.Segal DS, Kuczenski R. Repeated cocaine administration induces behavioral sensitization and corresponding decreased extracellular dopamine responses in caudate and accumbens. Brain Res. 1992;577:351–355. MEDLINE |
CrossRef
Segal and Mandell, 1974. 49.Segal DS, Mandell AJ. Long-term administration of d-amphetamine: progressive augmentation of motor activity and stereotypy. Pharmacol. Biochem. Behav. 1974;2:249–255. MEDLINE |
CrossRef
Shippenberg et al., 1996. 50.Shippenberg TS, Heidbreder C, Lefevour A. Sensitization to the conditioned rewarding effects of morphine: pharmacology and temporal characteristics. Eur. J. Pharmacol. 1996;299:33–39. MEDLINE |
CrossRef
Simonin et al., 2006. 51.Simonin F, Schmitt M, Laulin JP, Laboureyras E, Jhamandas JH, MacTavish D, et al. RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc. Natl. Acad. Sci. USA. 2006;103:466–471. MEDLINE |
CrossRef
Spanagel and Shippenberg, 1993. 52.Spanagel R, Shippenberg TS. Modulation of morphine-induced sensitization by endogenous kappa opioid systems in the rat. Neurosci. Lett. 1993;153:232–236. MEDLINE |
CrossRef
Stewart and Badiani, 1993. 53.Stewart J, Badiani A. Tolerance and sensitization to the behavioral effects of drugs. Behav. Pharmacol. 1993;4:289–312. Stinus et al., 1995. 54.Stinus L, Allard M, Gold L, Simonnet G. in CNS neuropeptide FF-like material, pain sensitivity, and opiate dependence following chronic morphine treatment. Peptides. 1995;16:1235–1241. MEDLINE |
CrossRef
Tang et al., 1984. 55.Tang J, Yang HY, Costa E. Inhibition of spontaneous and opiate mediated nociception by an andogenous neuropeptide with Phe-Met-Arg-Phe-NH2-like immunoreactivity. Proc. Natl. Acad. Sci. USA. 1984;81:5002–5005. MEDLINE |
CrossRef
Vezina et al., 1987. 56.Vezina P, Kalivas PW, Stewart J. Sensitization occurs to the locomotor effects of morphine and the specific mu opioid receptor agonist, DAGO, administered repeatedly to the ventral tegmental area but not to the nucleus accumbens. Brain Res. 1987;417:51–58. MEDLINE |
CrossRef
Walaas, 1981. 57.Walaas I. Biochemical evidence for overlapping neocortical and allocortical glutamate projections to the nucleus accumbens and rostral caudatoputamen in the rat brain. Neuroscience. 1981;6:399–405. MEDLINE |
CrossRef
Wise and Bozarth, 1987. 58.Wise RA, Bozarth MA. A psychomotor stimulant theory of addiction. Psychol. Rev. 1987;94:469–492.
CrossRef
Wolf and Jeziorski, 1993. 59.Wolf ME, Jeziorski M. Coadministration of MK-801 with amphetamine, cocaine or morphine prevents rather than transiently masks the development of behavioral sensitization. Brain Res. 1993;613:291–294. MEDLINE |
CrossRef
Wolf et al., 1995. 60.Wolf ME, Dahlin SL, Hu XT, Xue CJ, White K. Effects of lesions of prefrontal cortex, amygdala, or fornix on behavioral sensitization to amphetamine: comparison with N-methyl-d-aspartate antagonists. Neuroscience. 1995;69:417–439. MEDLINE |
CrossRef
Yang and Martin, 1995. 61.Yang HY, Martin RM. Isolation and characterization of a neuropeptide FF-like peptide from brain and spinal cord of rat. Soc. Neurosci. Abstr. 1995;21:760. Yang et al., 1985. 62.Yang HY, Fratta W, Majane EA, Costa E. Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc. Natl. Acad. Sci. USA. 1985;82:7757–7761. MEDLINE |
CrossRef
a Department of Pharmacology and Pharmacodynamics, Medical University, Staszica Str. 4, 20-081 Lublin, Poland b Faculty of Chemistry and Regional Laboratory, Jagiellonian University, Krakow, Poland  Corresponding author. Tel.: +48 81 5328927; fax: +48 81 5328903.
PII: S0143-4179(06)00115-6 doi:10.1016/j.npep.2006.09.048 © 2006 Elsevier Ltd. All rights reserved. | |
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