Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-13T03:18:34.314Z Has data issue: false hasContentIssue false

Cholecystokinin and panic disorder

Published online by Cambridge University Press:  24 June 2014

Michel Bourin*
Affiliation:
EA 3256 “Neurobiologie de l'Anxiété et de la Dépression”, Faculté de Médecine, Nantes cedex 1, France
Eric Dailly
Affiliation:
EA 3256 “Neurobiologie de l'Anxiété et de la Dépression”, Faculté de Médecine, Nantes cedex 1, France
*
Michel Bourin, EA 3256 “Neurobiologie de l'Anxiété et de la Dépression”, Faculté de Médecine, BP 53508, Nantes cedex 1, France. Tel: +33-2-40412852; Fax: +33-2-40412856; E-mail: mbourin@sante.univ-nantes.fr

Abstract

Evidence for implication of cholecystokinin (CCK) in the neurobiology of panic disorder is reviewed through animal and human pharmacological studies. The results of these investigations raise two issues: (i) selectivity of action of CCK-2 agonists in anxiety disorders; and (ii) aberrations of the CCK system in anxiety disorders, both of which are discussed.

Type
Review Article
Copyright
Copyright © 2004 Blackwell Munksgaard

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Dodd, J, Kelly, JS. Excitation of CA1 pyramidal neurones of the hippocampus by tetra- and octapeptide C-terminal fragments of cholecystokinin. J Physiol 1979;295: 6162. Google ScholarPubMed
Dodd, J, Kelly, JS. The actions of cholecystokinin and related peptides on pyramidal neurons of the mammalian hippocampus. Brain Res 1981;205: 337350.CrossRefGoogle ScholarPubMed
Boden, P, Hill, RG. Effects of cholecystokinin and related peptides on neuronal activity in the ventromedial nucleus of the rat hypothalamus. Br J Pharmacol 1988;94: 246252.CrossRefGoogle ScholarPubMed
Ishibaschi, S, Omura, Y, Okaijma, T, Shibata, S. Cholecytokinin, motilin and secretin effects on the central nervous system. Physiol Behav 1979;23: 401403.CrossRefGoogle Scholar
MacVicar, BA, Kerrin, JP, Davison, JS. Inhibition of synaptic transmission in the dorsal hippocampus by cholecystokinnin (CCK) and its antagonism by a CCK analog (CCK 27–33). Brain Res 1987;406: 130135.CrossRefGoogle Scholar
Lopes da Silva, FH, Witter, MP, Boeijinga, Ph, Lohman, AHM. Anatomical organization and physiology of limbic cortex. Physiol Rev 1990;70: 453511.Google Scholar
Pinget, M, Strauss, E, Yalow, RS. Localization of cholecystokinin-like reactivity in isolated nerve terminals. Proc Natl Acad Sci USA 1978;75: 63216326. CrossRefGoogle Scholar
Emson, PC, Lee, OM, Rehfeld, JF. Cholecystokinin octapeptide: vesicular localization and calcium dependent release from rat brain in vitro. Life Sci 1980;26: 21572163.CrossRefGoogle ScholarPubMed
Goltermann, NR, Rehfeld, JF, Roigaard-Petersen, H. In vivo biosynthesis of cholecystokinin in rat cerebral cortex. J Biol Chem 1980;255: 61816185.Google ScholarPubMed
Migaud, M, Durieux, C, Roques, BP. Evidences of cholecystokinin octapeptide (CCK8) uptake in rat cortex synaptosomal fractions. J Neurochem 1993;61(Suppl.): S83B. Google Scholar
Rehfeld, JF, Nielsen, FC. Molecular forms and regional distribution of cholecystokinin in the central nervous system. In: Bradwejn, J, Vasar, E, eds. Cholecystokinin and Anxiety: from Neuron to Behavior. Austin: R.G. Landes, 1995. Google Scholar
Hill, DR, Campbell, NJ, Shaw, TM, Woodruff, GN. Autoradioographic localization and biochemical characterization of peripherical type CCK receptors in rat CNS using highly selective non-peptide CCK agonists. J Neurosci 1987;7: 29672976.Google Scholar
Hill, DR, Shaw, TM, Graham, W, Woodruff, GN. Autoradiographical detection of cholecystokinin-A receptors in primate brain using 125l-Bolton-Hunter-CCK8 and 3H-MK-329. J Neurosci 1990;10: 10701081.Google ScholarPubMed
Gerhardt, GA, Friedmann, M, Brodie, MSet al. The effect of cholecystokinin (CCK8) on dopamine-containing nerve terminals in the caudale nucleus and nucleus accumbens of the anaesthelized rat in vivo electrochemical studies. Brain Res 1989;499: 157163.CrossRefGoogle Scholar
Vickroy, IW, Bianchi, BR. Pharmacological and mechanistic studies of cholecystokinin-facilitated 3H-dopamine efflux from rat nucleus accumbens. Neuropeptides 1989;13: 4350.CrossRefGoogle ScholarPubMed
Wank, SA, Harkins, R, Jensen, RT, Shapira, H, De Weerth, A, Slatter, T. Purification, molecular cloning, and functional expression of the cholecystokinin receptors from rat pancreas. Proc Natl Acad Sci USA 1992;89: 31253129.CrossRefGoogle ScholarPubMed
Ulrich, CD, Ferber, I, Hollcky, E, Hadac, E, Buell, G, Miller, LJ. Molecular cloning and functional expression of the human galibladder cholecystokinin A receptor. Biochem Biophys Res Commun 1993;193: 204211.CrossRefGoogle Scholar
Kopin, AS, Lee, Y-M, McBride, EWet al. Expression, cloning and characterization of the canine parietal cell gastrin receptor. Proc Natl Acad Sci USA 1992;89: 36053609.CrossRefGoogle ScholarPubMed
Lee, Y-M, Beinborn, M, McBride, EW, Lu, M, Kolakowski, LF, Kopin, AS. The human brain cholecystokinin-B/gastrin receptor. J Biol Chem 1993;268: 81648169.Google ScholarPubMed
Huppi, K, Siwarski Pisenga, JR, Wank, S. Chromosomal localization of the gastric and brain receptors for cholecystokinin (CCK-AR and CCK-BR) in human and mouse. Genomics 1995;25: 727729.CrossRefGoogle Scholar
Honda, I, Wada, H, Battey, JF, Wank, SA. Differential gene expression of CCK-A and CCK-B receptors in the rat brain. Mol Cell Neurosci 1993;4: 143154. CrossRefGoogle ScholarPubMed
Hahne, WF, Jensen, RT, Lemp, GF, Gardner, JD. Proglumide and benzotript: members of a different class of cholecystokinin receptor antagonists. Proc Natl Acad Sci USA 1981;78: 63046308.CrossRefGoogle ScholarPubMed
Chang, RSI, Lotti, VJ. Biochemical and pharmacological characterization of an extremely potent and selective nonpeptide cholecystokinin antagonist. Proc Natl Acad Sci USA 1986;83: 49234926.CrossRefGoogle ScholarPubMed
Gully, D, Frehel, D, Marcy, Cet al. Peripheral biological activity of SR 27897: a new potent non-peptide antagonist of CCK-A receptors. Eur J Pharmacol 1993;232: 1319.CrossRefGoogle Scholar
Lotti, VJ, Chang, RS L. A new and selective non-peptide gastrin antagonist and brain cholecystokinin receptor (CCK-B) ligand: L-365,260. Eur J Pharmacol 1989;162: 273280.CrossRefGoogle ScholarPubMed
Hughes, J, Boden, P, Costall, Bet al. Development of a class of selective cholecystokinin type B receptor antagonists having potent anxiolytic activity. Proc Natl Acad Sci USA 1990;87: 67286732.CrossRefGoogle ScholarPubMed
Howbert, JJ, Lobb, KL, Brown, RFet al. A novel series of non-peptide CCK and gastrin antagonists: medicinal chemistry and electrophysiological demonstration of antagonism. In: Dourish, CT, Cooper, SJ, Iversen, SD, Iversen, LL, eds. Multiple Cholecystokinin Receptors in the CNS. New York: Oxford University Press, 1992. Google Scholar
Bertrand, P, Bohme, GA, Durieux, Cet al. Pharmacological properties of urido-acetamides, new potent and selective non-peptide CCK-B/gastrin receptor antagonists. Eur J Pharmacol 1994;262: 233245.CrossRefGoogle Scholar
Bourin, M. Cholecystokinin as a target for neuropsychiatric drugs. Drug News Perspect 1998;11: 342349. CrossRefGoogle ScholarPubMed
Bourin, M, Malinge, M, Vasar, E, Bradwejn, J. Two faces of cholecystokinin: anxiety and schizophrenia. Fundam Clin Pharmacol 1996;10: 116120.CrossRefGoogle Scholar
Shlik, J, Vasar, E, Bradwejn, J. Cholecytokinin and psychiatric disorders: role in aetiology and potential of receptor antagonist in therapy. CNS Drugs 1997;8: 134152. CrossRefGoogle Scholar
Dawson, GR, Rupniak, NMJ, Iversen, SDet al. Lack of effect of CCK-B receptor antagonists in ethological and conditioned animal screens for anxiolytic drugs. Psychopharmacology 1995;121: 109117.CrossRefGoogle Scholar
Köks, S, Mannistô, T, Bourin, M, Shlik, J, Vasar, V, Vasar, E. Cholecystokinine (CCK) induced anxiety in rats: relevance of preexperimental stress and seasonal variations. J Psychiatr Neurosc 2000;25: 3342. Google Scholar
Bradwejn, J, De Montigny, C. Benzodiazepines antagonise cholecystokinin-induced activation of rat hippocampal neurons. Nature 1984;312: 363364.CrossRefGoogle Scholar
de Montigny, C. Cholecytokinin tetrapeptide induces panic-like attacks in healthy volunteers. Arch General Psychiat 1989;46: 511517. CrossRefGoogle Scholar
Bradwejn, J, Koszycki, D, Meterissian, G. Cholecystokinin-tetrapeptide in panic disorder. Can J Psychiat 1990;35: 8385. CrossRefGoogle ScholarPubMed
Bradwejn, J, Koszycki, D, Shriqui, C. Enhanced sensitivity to cholecystokinin tetrapeptide in panic disorder. Arch General Psychiatry 1991;48: 603610. CrossRefGoogle ScholarPubMed
Abelson, JL, Nesse, RM, Vinik, A. Stimulation of corticotrophin release by pentagastrin in normal subjects and patients with panic disorder. Biol Psychiatry 1991;29: 12201223.CrossRefGoogle ScholarPubMed
Van Megen, HJGM, Westenberg, HGM, Den Boer, JA, Haigh, JRM, Traub, M. Pentagastrin induced panic attacks: enhanced sensitivity in panic disorder patients. Psychopharmacology 1994;114: 10211033. CrossRefGoogle ScholarPubMed
Lydiard, RB, Ballenger, JC, Laraia, MT, Fossey, MD, Beinfeld, MC. CSF cholecystokinin concentrations in patients with panic disorder and in normal comparison subjects. Am J Psychiat 1992;149: 691693.Google ScholarPubMed
Brambilla, F, Bellodi, L, Perna, G, Garberi, A, Sacerdote, P. Lymphocyte cholecytokinin concentrations in panic disorder. Am J Psychiat 1993;150: 11111113.Google Scholar
Bradwejn, J, Koszycki, D, Couëtoux du Tertre, A, Van Megen, H, Den Boer, J, Westenberg, H, Annable, L. The panicogenic effects of cholecystokinin tetrapeptide are antagonised by L-365.260, a central cholecystokinin receptor antagonist, in patients with panic disorder. Arch General Psychiat 1994;51: 486493. CrossRefGoogle Scholar
Bradwejn, J. Cholecystokinin and panic disorder. In: Bradwejn, J, Vasar, E, eds. Cholecystokinin and Anxiety: from Neuron to Behavior. Austin: RG Landes, 1995. CrossRefGoogle Scholar
Bradwejn, J, Koszycki, D. Imipramine antagonises the panicogenic effects of CCK4 in panic disorder patients. Am J Psychiat 1994;151: 261263. Google Scholar
Kramer, MS, Cutler, NR, Ballenger, JCet al. A placebo-controlled trial of L-365,260, a CCKB antagonist, in panic disorder. Biol Psychiatry 1995;37: 462466.CrossRefGoogle ScholarPubMed
Flint, AJ, Koszycki, D, Bradwejn, J, Vaccarino, FJ. Neurohormonal responses to cholecystokinin tetrapeptide: a comparison of younger and older healthy subjects. Psychoneuroendocrinology 2000;25: 633647.CrossRefGoogle ScholarPubMed
Ströhle, A, Holsboer, F, Rupprecht, R. Increased ACTH concentrations associated with cholecystokinin tetrapeptide-induced panic attacks in patients with panic disorder. Neuropsychopharmacology 2000;22: 251256.CrossRefGoogle ScholarPubMed
Flint, AJ. Epidemiology and comorbidity of anxiety disorders in the elderly. Am J Psychiatry 1994;151: 640649.Google ScholarPubMed
Flint, A, Bradwejn, J, Vaccarino, F, Gutkowska, J, Palmour, R, Koszycki, D. Aging and panicogenic response to cholecystokinin tetrapeptide: an examination of the cholecystokinin system. Neuropsychopharmacology 2002;27: 663671.Google ScholarPubMed
Bourin, M, Baker, GB, Bradwejn, J. Neurobiology of panic disorder. J Psychosom Res 1998;44: 161180. CrossRefGoogle ScholarPubMed
Männisto, PT, Lang, A, Harro, J, Peuranen, E, Bradwejn, J, Vasar, E. Opposite effects mediated by CCKA and CCKB receptors in behavioural and hormonal studies in rats. Naunyn Schmiedebergs Arch Pharmacol 1994;349: 478484.CrossRefGoogle ScholarPubMed
Hattori, E, Ebihara, M, Yamada, K, Ohba, H, Shibuya, H, Yoshikawa, T. Identification of a compound short tandem repeat stretch in the 5′-upstream region of the cholecystokinin gene, and its association with panic disorder but not with schizophrenia. Mol Psychiatry 2001;6: 465470.CrossRefGoogle Scholar
Hamilton, SP, Slager, SL, Helleby, Let al. No association or linkage between polymorphisms in the genes encoding cholecystokinin and the cholecystokinin B receptor and panic disorder. Mol Psychiatry 2001;6: 5965.CrossRefGoogle ScholarPubMed
Ise, K, Akiyoshi, J, Horinouchi, Y, Tsutsumi, T, Isogawa, K, Nagayama, H. Association between the CCK-A receptor gene and panic disorder. Am J Med Genet 2003;118B: 2931.CrossRefGoogle ScholarPubMed
Hattori, E, Yamada, K, Toyota, Tet al. Association studies of the CT repeat polymorphism in the 5′ upstream region of the cholecystokinin B receptor gene with panic disorder and schizophrenia in Japanese subjects. Am J Med Genet 2001;105: 779782.CrossRefGoogle ScholarPubMed
Kennedy, JL, Bradwejn, J, Koszycki, Det al. Investigation of cholecystokinin system genes in panic disorder. Mol Psychiatry 1999;4: 284285.CrossRefGoogle ScholarPubMed
Harro, J, Vasar, E, Bradwejn, J. CCK in animal and human research on anxiety. Trends Pharmacol Sci 1993;14: 244249.CrossRefGoogle ScholarPubMed
Branchereau, P, Bohme, GA, Champagnat, Jet al. CholecystokininA and cholecystokininB receptors in neurons of the brainstem solitary complex of the rat: pharmacological identification. J Pharmacol Exp Ther 1992;260: 14331440.Google ScholarPubMed
Vasar, E, Lang, A, Harro, Jet al. Subdiaphragmatic vagotomy does not prevent the anti-exploratory effect of caerulein in the elevated plus-maze. Neuropeptides 1994;26: 3945.CrossRefGoogle Scholar
Bradwejn, J, Legrand, JM, Koszycki, D, Bates, J, Bourin, M. Effects of cholecystokinin tetrapeptide on respiratory function in healthy volunteers. Am J Psychiat 1998;155: 280282.Google ScholarPubMed
Bradwejn, J, Koszycki, D, Couetoux Du Tertre, A, Bourin, M, Palmour, R, Ervin, F. The cholecystokinin hypothesis of panic anxiety disorders: a review. J Psychopharmacol 1992;6: 345351. CrossRefGoogle ScholarPubMed
Beinfeld, MC, Meyer, DK, Eskay, RL, Jensen, RT, Brownstein, MJ. The distribution of cholecystokinin immunoreactivity in the central nervous system of the rat as determined by radioimmunoassay. Brain Res 1981;212: 5157.CrossRefGoogle ScholarPubMed
Tang, F, Man, WS. The regional distribution of thyrotropin releasing hormone, leu-enkephalin, met-enkephalin, substance P, somatostatin and cholecystokinin in the rat brain and pituitary. Neuropeptides 1991;19: 287292.CrossRefGoogle ScholarPubMed
Swanson, LW, Lind, RW. Neural projections subserving the initiation of a specific motivated behavior in the rat: new projections from the subfornical organ. Brain Res 1986;379: 399403.CrossRefGoogle ScholarPubMed
Mezey, E, Reisine, TD, Skirboll, L, Beinfeld, M, Kiss, JZ. Role of cholecystokinin in corticotropin release: coexistence with vasopressin and corticotropin-releasing factor in cells of the rat hypothalamic paraventricular nucleus. Proc Natl Acad Sci USA 1986;83: 35103512.CrossRefGoogle ScholarPubMed
Reisine, T, Jensen, R. Cholecystokinin-8 stimulates adrenocorticotropin release from anterior pituitary cells. J Pharmacol Exp Ther 1986;236: 621626.Google ScholarPubMed
Kamilaris, TC, Johnson, EO, Calogero, AEet al. Cholecystokinin-octapeptide stimulates hypothalamic-pituitary-adrenal function in rats: role of corticotropin-releasing hormone. Endocrinology 1992;130: 17641774.Google ScholarPubMed
Morley, JE, Melmed, S, Briggs, Jet al. Cholecystokinin octapeptide releases growth hormone from the pituitary in vitro. Life Sci 1979;25: 12011205.CrossRefGoogle ScholarPubMed
Vijayan, E, Samson, WK, McCann, SM. In vivo and in vitro effects of cholecystokinin on gonadotropin, prolactin, growth hormone and thyrotropin release in the rat. Brain Res 1979;172: 295302.CrossRefGoogle ScholarPubMed
Singh, L, Field, MJ, Hughes, Jet al. The behavioural properties of CI-988, a selective cholecystokininB receptor antagonist. Br J Pharmacol 1991;104: 239245.CrossRefGoogle ScholarPubMed
Harro, J, Lofberg, C, Rehfeld, JF, Oreland, L. Cholecystokinin peptides and receptors in the rat brain during stress. Naunyn Schmiedebergs Arch Pharmacol 1996; 354: 5966.CrossRefGoogle ScholarPubMed
Pavlasevic, S, Bednar, I, Qureshi, GA, Sodersten, P. Brain cholecystokinin tetrapeptide levels are increased in a rat model of anxiety. Neuroreport 1993;5: 225228.CrossRefGoogle Scholar
Branchereau, P, Champagnat, J, Roques, BP, Denavit-Saubie, M. CCK modulates inhibitory synaptic transmission in the solitary complex through CCKB sites. Neuroreport 1992; 3: 909912.CrossRefGoogle ScholarPubMed
Philipp, E, Wilckens, T, Friess, E, Platte, P, Pirke, KM. Cholecystokinin, gastrin and stress hormone responses in marathon runners. Peptides 1992;13: 125128.CrossRefGoogle ScholarPubMed
Harro, J, Oreland, L, Vasar, E. cholecystokinin receptors and animal models of anxiety. Clin Neuropharmacol 1992;15(Suppl.)1Pt A: 479480A. CrossRefGoogle ScholarPubMed
Feldman, M, Walker, P, Goldschmiedt, M, Cannon, D. Role of affect and personality in gastric acid secretion and serum gastrin concentration. Comparative studies in normal men and in male duodenal ulcer patients. Gastroenterology 1992;102: 175180.CrossRefGoogle ScholarPubMed
Fekete, M, Rentzsch, A, Schwarzberg, H, Telegdy, G. Effect of cholecystokinin on self-stimulation behavior in rats. Eur J Pharmacol 1983;91: 7782.CrossRefGoogle ScholarPubMed
Harro, J, Kliivet, RA, Lang, A, Vasar, E. Rats with or without anxious or non- anxious type of exploratory behavior differ in their brain CCK-8 and benzodiazepine receptor characteristics. Behav Brain Res 1990;39: 6371.CrossRefGoogle ScholarPubMed
Vasar, E, Peuranen, E, Oopik, T, Harro, J, Mannisto, PT. Ondansetron, an antagonist of 5-HT3 receptors, antagonizes the anti-exploratory effect of caerulein, an agonist of CCK receptors, in the elevated plus-maze. Psychopharmacology (Berl) 1993;110: 213228.CrossRefGoogle ScholarPubMed
Costall, B, Domeney, AM, Kelly, MEet al. The effect of the 5-HT3 receptor antagonist, RS-42358–197, in animal models of anxiety. Eur J Pharmacol 1993;234: 9199.CrossRefGoogle ScholarPubMed