Introduction adrenals [5,7,8,15,24,27,28,39]. The mature CART peptide

Brain Research 887 2000 125–133 www.elsevier.com locate bres Research report Effects of CART peptides on food consumption, feeding and associated behaviors in the goldfish, Carassius auratus: actions on neuropeptide Y- and orexin A-induced feeding ´ ` Helene Volkoff, Richard Ector Peter Department of Biological Sciences , University of Alberta, Edmonton, Alb., Canada T6G 2E9 Accepted 19 September 2000 Abstract CART cocaine- and amphetamine-regulated transcript peptides are novel brain neuropeptides that have been shown to have a role in the control of feeding behavior in mammals. The effects of intracereboventricular i.c.v. administration of two CART fragments, CART 62–76 and CART 55–102 on feeding and behavioral activity of goldfish Carassius auratus were examined. Both CART peptide fragments inhibited food intake in goldfish. Co-injection of CART peptide and neuropeptide Y NPY reduced the increase in feeding caused by injection of NPY alone. CART 55–102 was more potent than CART 62–76. Co-treatment with CART 55–102 and orexin A inhibited the feeding response induced by orexin A alone. Feeding behavior was stimulated relative to saline controls following injection of CART 62–76 alone and co-injection of NPY and CART 62–76, but was not affected by treatment with CART 55–102 alone, NPY and CART 55–102 or orexin A and CART 55–102. Total behavioral activity was increased with NPY, orexin A, and both CART fragments alone as compared to saline controls, as well as in fish co-treated with NPY and CART 62–76 or NPY and CART 55–102 as compared to saline controls and NPY-treated fish. Tremors were seen in fish treated with CART 55–102 alone, and in fish co-treated with NPY and CART 55–102 and orexin A and CART 55–102. Co-treatment of the fish with NPY but not with orexin A significantly lowered the frequency of fish showing tremors as compared to fish treated with CART alone. These results indicate that CART peptides are involved in the regulatory pathways of feeding and behavioral activity in goldfish.  2000 Elsevier Science B.V. All rights reserved. Theme : Neural basis of behavior Topic : Neuropeptides and behavior Keywords : CART peptide; Neuropeptide Y; Orexin A; Feeding behavior; Behavioral activity; Goldfish 1. Introduction adrenals [5,7,8,15,24,27,28,39]. The mature CART peptide contains either 102 long form or 89 short form amino CART cocaine- and amphetamine-regulated transcript acid residues and has several potential cleavage sites [14]. peptides are recently characterized neuropeptides that have The processing of CART peptides is tissue-specific been implicated in the control of appetite in mammals. [31,44]. To date, at least six CART peptides have been CART was initially isolated using PCR differential display identified in mammals [1,31]. as mRNA produced primarily in the rat striatum and In mammals, CART is expressed in hypothalamic areas transcriptionally up-regulated by acute administration of implicated in the control of feeding behavior, such as the psychomotor stimulants such as cocaine and amphetamine arcuate and paraventricular nucleus [2,3,9,14,16,20,28] and [13]. CART was later found to be present throughout its mRNA expression is lowered in fasting conditions mammalian brain and in pituitary, gut, pancreas, and [2,29]. In addition, the gastrointestinal tract contains CART immunoreactivity [8]. In rodents, intracerebroven- tricular injections of CART fragments have been shown to Corresponding author. Tel.: 11-780-492-5685; fax: 11-780-492- inhibit both normal and starvation-induced feeding in a 7033. E-mail address : dick.peterualberta.ca R.E. Peter. dose-dependent manner [3,29,32,47]. CART 55–102, a 0006-8993 00 – see front matter  2000 Elsevier Science B.V. All rights reserved. P I I : S 0 0 0 6 - 8 9 9 3 0 0 0 3 0 0 1 - 8 126 H naturally occurring fragment isolated from ovine hypo- pellets Moore Clark, St. Andrews, NB, Canada. Fish thalamus [40] appears to be the most potent fragment. The were acclimated under these standard conditions for ap- numbers in the fragments derive from the predicted signal proximately 2 weeks before the start of an experiment. peptide cleavage site in the long form of CART [14]. Other Forty-eight hours prior to experimentation, two fish were CART fragments including CART 54–105, CART 60– moved into an observation tank and starved. 105, CART 61–105 [43], CART 55–76 and CART 62–76 [32] have also been shown to cause a dose- 2.2. Intracerebroventricular i.c.v. injections dependent feeding inhibition in rats. Immunoneutralization of CART by administration of rabbit anti-CART 55–102 Brain i.c.v. injections were administered following results in higher food intake in rats, suggesting that CART . procedures described by Peter and Gill [37] Briefly, is an endogenous satiety factor [32,42]. following deep anesthesia, a three-sided flap was cut in the NPY-containing terminals are present around CART roof of the skull using a dentist drill equipped with a peptide-positive cell bodies in the paraventricular nucleus circular saw. The flap was then folded to the side, exposing of the hypothalamus [3,9,32] suggesting a regulation of the brain. Fish were then placed in a specially designed NPY on CART output. Decreased levels of the adipocyte stereotaxic apparatus. The needle of a 5-ml microsyringe hormone leptin, as seen during fasting or in obese rats with was stereotaxically placed in the preoptic region of the impaired leptin action, cause a fall in the expression of brain third ventricle according to coordinates 11.0, M, D CART mRNA [2,48] which can be restored by peripheral 1.2 taken from the stereotaxic atlas of the goldfish brain administration of leptin [29]. Leptin treatment activates [37]. Following injection of 2 ml of test solution, the CART hypothalamic neurons [16]. In turn, intracereb- needle was withdrawn and the space in the cranial cavity roventricular injection of recombinant CART inhibits filled with teleost physiological saline [4]. The skull flap NPY-induced feeding [32]. was put back in place, and secured by surgical thread. Fish In fish, there is limited information on the neural control were then returned to their tanks, and normally recovered of feeding behavior. Recent studies show that orexigenic from anesthesia within 2–5 min. All experiments were peptides such as NPY [33,35], galanin [10], and orexins carried out in accordance with the principles published in [46], and anorexigenic peptides such as corticotropin-re- the Canadian Council on Animal Care’s ‘‘guide to the care leasing factor Bernier, Andrusky, Volkoff and Peter, and use of experimental animals’’. unpublished; [11], cholecystokinin [20], serotonin [12] and bombesin [19] are involved in the regulation of feeding in goldfish. 2.3. Observational experiments To determine if CART peptides are involved in feeding in goldfish, we tested the effects of different doses of two Fish were tested in random order in terms of treatment recombinant CART fragments, CART 62–76 and CART and days. For each experiment, two fish were placed in a 55–102, on the feeding behavior of food-restricted fish single observation tank to avoid stress due to isolation and and in fish subjected to NPY- or orexin A OXA-induced to allow for an accurate observation of feeding behavior feeding. As CART peptides might have various physiolog- and food consumption. Observations were made for each ical functions and influence other behaviors besides feed- individual fish. An approximate 4 bw ration of pellets ing, we also examined the effects of CART fragments on per fish was administered at 15 min post-injection. Be- behavioral activity. havioral observations and measurement of food consump- tion commenced upon entry of pellets into the tank, and were made for 1 h. Observations were divided in 15-min

2. Material and methods periods. Feeding behavior was assessed by counting the