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Behavioral Effects of Central Administration of the Novel CRF Antagonist Astressin in Rats Mariarosa G

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Behavioral Effects of Central Administration of the Novel CRF Antagonist Astressin in Rats Mariarosa G Behavioral Effects of Central Administration of The Novel CRF Antagonist Astressin in Rats Mariarosa G. Spina, Ph.D., Ana M. Basso, Ph.D., Eric P. Zorrilla, Ph.D., Charles J. Heyser, Ph.D., Jean Rivier, Ph.D., Wylie Vale, Ph.D., Emilio Merlo-Pich, M.D., and G.F. Koob, Ph.D. Astressin, a novel corticotropin releasing factor (CRF) a familiar environment. When these results were compared antagonist, has been found to be particularly potent at to previous studies performed with the same paradigms inhibiting the hypothalamo-pituitary-adrenal axis. The aim using other CRF antagonists, astressin showed effects of the present study was to determine the effects in rats of similar to those of D-PheCRF(12-41) on plus-maze ␣ astressin in attenuating the anxiogenic-like response performance. However, contrary to -helicalCRF(9-41) and produced by social stress and intracerebroventricular D-PheCRF(12-41), astressin had no effect on CRF-induced (ICV) CRF administration on the elevated plus-maze, and locomotor activity. These results suggest that astressin ICV CRF-induced locomotor activation in the rat. may have a unique anti-CRF profile compared to Astressin significantly reversed the anxiogenic-like previously tested antagonists. response induced by both social stress and ICV rat/ [Neuropsychopharmacology 22:230–239, 2000] humanCRF (r/hCRF) on the elevated plus-maze, but failed © 2000 American College of Neuropsychopharmacology. to block the effects of r/hCRF-induced locomotor activity in Published by Elsevier Science Inc. KEY WORDS: Astressin; CRF-antagonists; r/hCRF; Social al. 1981). Many studies have shown that CRF also exerts stress; Anxiety; Elevated plus-maze; Locomotor activity a number of autonomic and behavioral responses to stress independent of the pituitary adrenal-axis (Vale et al. Corticotropin-releasing factor (CRF) is a 41 amino acid 1983; Dunn and Berridge 1990; Koob et al. 1993). This ev- peptide, first isolated from ovine hypothalamus and re- idence supports the development of synthetic CRF ana- sponsible for the regulation of the pro-opiomelanocortin- logs of potential psychotherapeutic relevance. A family derived peptides secreted by the pituitary gland (Vale et of structurally constrained and long-acting CRF an- ␣ ␣ tagonists, such as -helicalCRF(9-41) [ -helCRF(9-41)] and D-PheCRF(12-41), has been identified and studied (Rivier From the Institute for Medical Neurobiology (MGS), Otto-von- et al. 1984; Tazi et al. 1987; Baldwin et al. 1991, Rivier et al. Guericke University, Magdeburg, Germany; Departamento de Farmacologia (AMB), Facultad de Ciencias Quimicas, Universidad 1993; Hernandez et al. 1993). In particular, in vivo studies de Cordoba, Cordoba, Argentina; Division of Psychopharmacology of the effects of D-PheCRF(12-41), injected directly into the (EPZ, GFK), Department of Neuropharmacology, The Scripps cerebral ventricle, showed a powerful and prolonged bi- Research Institute, La Jolla, California, USA; Department of Psy- chology (CJH), Franklin and Marshall College, Lancaster, Pennsyl- ological action compared to other CRF analogs (Curtis et vania, USA; Clayton Laboratories for Peptide Biology (JR, WV), The al. 1994; Menzaghi et al. 1994; Takahashi et al. 1989; Rod- Salk Institute, La Jolla, California, USA; Department of Pharmacol- riguez de Fonseca et al. 1996). ogy (EM-P), Glaxo-Wellcome Richerche, Verona, Italy. Received April 9, 1999; revised July 21, 1999; accepted August 20, Recently, a new member of the CRF-modified analog 1999. of D-PheCRF(12-41), astressin (see Table 1), has been syn- Address correspondence to: Dr. George F. Koob, Department of thesized and tested in vitro (Gulyas et al. 1995; Aubry et Neuropharmacology, CVN-7, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037. Fax: 858-784-7405. al. 1997) and in vivo (Gulyas et al. 1995; Baram et al. E-mail: [email protected] 1996; Martinez et al. 1997, 1998; Rivier et al. 1996; NEUROPSYCHOPHARMACOLOGY 2000–VOL. 22, NO. 3 © 2000 American College of Neuropsychopharmacology Published by Elsevier Science Inc. 0893-133X/00/$–see front matter 655 Avenue of the Americas, New York, NY 10010 PII S0893-133X(99)00108-6 NEUROPSYCHOPHARMACOLOGY 2000–VOL. 22, NO. 3 Effects of Astressin in Rats 231 Maecker et al. 1997; Lee and Rivier 1997; Turnbull et al. hour light/dark cycle (lights on at 6:00 AM). Animals 1999; Ando et al. 1998). This peptide presents an ␣-heli- had free access to standard rat food and tap water. The cal structure common to previously synthesized ana- rats were allowed a 1-week period of acclimation to the logs. However, it also includes a bridge between the 30 animal room and were handled once before surgery. A and 33 amino acid within the sequence, which may ac- total of 307 rats were used for this study. Animals first count for the higher affinity for CRF receptors (Gulyas were tested on the elevated plus-maze. et al. 1995, Miranda et al. 1997). In a pituitary cell cul- ture assay, astressin has been found to be 100 times ␣ more potent than -helCRF(9-41) and 32 times more po- Surgery tent than D-PheCRF in blocking CRF-induced (12-41) Animals were anesthetized with halothane and placed ACTH release (Gulyas et al. 1995). Furthermore, as- in a Kopf stereotaxic instrument. Stainless steel guide tressin was 10 times more potent than ␣-helCRF and (9-41) cannulae (23 gauge, 7-mm long) were implanted unilat- D-PheCRF in vivo in blocking the ACTH secretion (12-41) erally, 1 mm above the lateral ventricle (AP Ϫ0.6 mm, L ϩ induced by adrenalectomy or electroshock (Gulyas et al. or Ϫ2.0 mm from bregma, and DV Ϫ3.2 mm from the 1995). In the rat, pretreatment with astressin produced a point of entry, according to Pellegrino et al. 1979). The marked inhibition of both CRF- and urocortin-induced cannula was secured to the skull using four stainless increases in plasma ACTH levels (Turnbull et al. 1999). steel screws and dental cement and closed with a re- The aim of the present study was to characterize the movable stylet. Animals were allowed a 1-week recov- central effects of astressin and its ability to antagonize ery period before testing. the behavioral response to stress and to antagonize ex- ogenous administration of rat/human CRF (r/hCRF). The properties of astressin to reverse social defeat stress Peptides and ICV Injections and intracerebroventricular (ICV) CRF-induced anxio- genic-like responses, reflected in a decrease in explor- Astressin [cyclo(30-33) [D-Phe12, Nle21-38, Glu30,Lys33]- ␣ atory behavior of the open arms of the elevated plus- hCRF(12-41)], D-PheCRF(12-41) and -helCRF(9-41) were dis- maze, and to block the locomotor activity induced by solved in double-distilled water (pH 6.7), and r/hCRF ICV administration of r/hCRF in a familiar environ- was dissolved in sterile saline just before the start of ment, were tested. The dose range of astressin used was each experiment and kept on ice. Both peptides were selected according to previous studies in which the CRF provided by the Clayton Foundation Laboratories for ␣ antagonists D-PheCRF(12-41) and -helCRF(9-41) were Peptide Biology, The Salk Institute (La Jolla, CA). Rats used in the same testing conditions (Heinrichs et al. were injected ICV by gravity using an 8.5-mm long in- 1992; Merlo-Pich et al. 1993; Menzaghi et al. 1994) and jector, connected to calibrated polyethylene 10 tubing. according to in vitro potency data (Gulyas et al. 1995). The tubing was raised above the head of the rat until 2 or 5 ␮l of CRF or astressin, respectively, were infused and then lowered to the height of the cannula for a 30- MATERIAL AND METHODS second waiting period after the end of the injection to prevent backflow leakage. The injector was removed Subjects and replaced by a stylet. After at least a one week inter- Male Wistar rats (Charles River Laboratories, Kingston, val from the first experiment, animals were tested for NY), weighing 250 Ϯ 20 g at the start of the experi- locomotor activity. The position of the ICV cannula was ments, were housed three per cage and maintained in a verified by gravity injection of blue dye at the comple- temperature- and light-controlled environment on a 12- tion of each experiment. Table 1. Amino Acid Sequence of CRF-Derived Synthetic Peptides with Antagonistic Properties ␣ ␣ -helicalCRF(9-41) -helCRF(9-41) D-L-T-F-H-L-L-R-E-M-L-E-M-A-K-A-E-Q-E-A-E-Q-A-A-L-N-R-L-L-L-E-E-A-NH2 (Rivier et al. 1984) 12 21,38 37 [D-Phe , Nle , CMeLeu ]rCRF(12-41) D-PheCRF(12-41) D-Phe-H-L-L-R-E-V-L-E-Nle-A-R-A-E-Q-L-A-Q-Q-A-H-S-N-R-K-MeLeu-Nle-E-I-I-NH2 (Hernandez et al, 1993) 12 21,38 30 33 Cyclo(30-33)[D-Phe , Nle , Glu ,Lys ]rCRF(12-41) astressin D-Phe-H-L-L-R-E-V-L-E-Nle-A-R-A-E-Q-L-A-Q-Glu-A-H-Lys-N-R-K-L-Nle-E-I-I-NH2 (Gulyas et al. 1995) ␣ A family of structurally constrained and long-acting CRF antagonists: -helCRF(9-41), D-PheCRF(12-41), and the new member of the CRF modified an- alog of D-PheCRF(12-41), astressin. 232 M.G. Spina et al. NEUROPSYCHOPHARMACOLOGY 2000–VOL. 22, NO. 3 Social Stress the cage, 2 cm above the floor and 16 cm from one an- other. Beam interruptions were recorded by a computer This procedure was used to stress the animals before and printed out every 10 minutes.
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