Anxiety-like behavior and locomotion in CCK1 knockout rats as a function of strain, sex and early maternal environment

Behavioural Brain Research

Volumn 211, Issue 2, 2010, Pages 198-207

  Schroeder, Mariana ^a   Weller, Aron ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Anxiety; Cholecystokinin (CCK); Elevated plus maze; Locomotion; Open field; Rats

Indexed keywords

CHOLECYSTOKININ; CORTICOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FEMALE; FOSTER CARE; GROOMING; LOCOMOTION; MALE; MAZE TEST; MUSCLE STRAIN; NONHUMAN; OPEN FIELD TEST; OTSUKA LONG EVANS TOKUSHIMA FATTY RAT; PHENOTYPE; PRIORITY JOURNAL; RAT; SEX;

ANIMALS; ANXIETY; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; MALE; MATERNAL BEHAVIOR; MAZE LEARNING; MOTOR ACTIVITY; RATS; RATS, INBRED OLETF; RATS, LONG-EVANS; RATS, MUTANT STRAINS; RECEPTOR, CHOLECYSTOKININ A; RECEPTOR, CHOLECYSTOKININ B; SEQUENCE DELETION; SEX FACTORS; SOCIAL ENVIRONMENT; SPECIES SPECIFICITY;

EID: 77952419492     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.03.038     Document Type: Article

References (70)

1. Akiyoshi J., Isogawa K., Tsutsumi T., Kasturagi S., Kohno K., Furuta M., et al. Cholecystokinin tetrapeptide-induced calcium mobilization in T cells of patients with panic disorder, major depression, or schizophrenia. Biol Psychiatry 1997, 42:151-154.
2. Akiyoshi J., Moriyama T., Isogawa K., Miyamoto M., Sasaki I., Kuga K., et al. CCK-4-induced calcium mobilization in T cells is enhanced in panic disorder. J Neurochem 1996, 66:1610-1616.
3. Alho H., Ferrarese C., Vicini S., Vaccarino F. Subsets of GABAergic neurons in dissociated cell cultures of neonatal rat cerebral cortex show co-localization with specific modulator peptides. Brain Res 1988, 467:193-204.
4. Ballaz S., Barber A., Fortuno A., Del Rio J., Martin-Martinez M., Gomez-Monterrey I., et al. Pharmacological evaluation of IQM-95,333, a highly selective CCKA receptor antagonist with anxiolytic-like activity in animal models. Br J Pharmacol 1997, 121:759-767.
5. Beinfeld M.C., Palkovits M. Distribution of cholecystokinin (CCK) in the rat lower brain stem nuclei. Brain Res 1982, 238:260-265.
6. Blass E.M., Shide D.J. Endogenous cholecystokinin reduces vocalization in isolated 10-day-old rats. Behav Neurosci 1993, 107(3):488-492.
7. Braw Y., Malkesman O., Dagan M., Bercovich A., Lavi-Avnon Y., Schroeder M., et al. Anxiety-like behaviors in pre-pubertal rats of the Flinders Sensitive Line (FSL) and Wistar-Kyoto (WKY) animal models of depression. Behav Brain Res 2006, 167:261-269.
8. Caldji C., Diorio J., Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 2000, 48:1164-1174.
9. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 1998, 95:5335-5340.
10. Champagne F., Meaney M.J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 2001, 133:287-302.
11. Champagne F.A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 2008, 29:386-397.
12. Chang R.S., Lotti V.J. Biochemical and pharmacological characterization of an extremely potent and selective nonpeptide cholecystokinin antagonist. Proc Natl Acad Sci USA 1986, 83:4923-4926.
13. Cohen H., Kaplan Z., Matar M.A., Buriakovsky I., Bourin M., Kotler M. Different pathways mediated by CCK1 and CCK2 receptors: effect of intraperitonal mrna antisense oligodeoxynucleotides to cholecystokinin on anxiety-like and learning behaviors in rats. Depress Anxiety 2004, 20:139-152.
14. Costall B., Domeney A.M., Hughes J., Kelly M.E., Naylor R.J., Woodruff G.N. Anxiolytic effects of CCK-B antagonists. Neuropeptides 1991, 19(Suppl.):65-73.
15. Crawley J.N. Cholecystokinin-dopamine interactions. Trends Pharmacol Sci 1991, 12:232-236.
16. Crawley J.N. Comparative distribution of cholecystokinin and other neuropeptides. Why is this peptide different from all other peptides?. Ann NY Acad Sci 1985, 448:1-8.
17. Crawley J.N. Subtype-selective cholecystokinin receptor antagonists block cholecystokinin modulation of dopamine-mediated behaviors in the rat mesolimbic pathway. J Neurosci 1992, 12:3380-3391.
18. Crawley J.N., Corwin R.L. Biological actions of cholecystokinin. Peptides 1994, 15:731-755.
19. Crespi F. The role of cholecystokinin (CCK), CCK-A or CCK-B receptor antagonists in the spontaneous preference for drugs of abuse (alcohol or cocaine) in naive rats. Methods Find Exp Clin Pharmacol 1998, 20:679-697.
20. Crespi F., Corsi M., Reggiani A., Ratti E., Gaviraghi G. Involvement of cholecystokinin within craving for cocaine: role of cholecystokinin receptor ligands. Expert Opin Investig Drugs 2000, 9:2249-2258.
21. Dauge V., Bohme G.A., Crawley J.N., Durieux C., Stutzmann J.M., Feger J., et al. Investigation of behavioral and electrophysiological responses induced by selective stimulation of CCKB receptors by using a new highly potent CCK analog, BC 264. Synapse 1990, 6:73-80.
22. Dauge V., Steimes P., Derrien M., Beau N., Roques B.P., Feger J. CCK8 effects on motivational and emotional states of rats involve CCKA receptors of the postero-median part of the nucleus accumbens. Pharmacol Biochem Behav 1989, 34:157-163.
23. de Montigny C. Cholecystokinin tetrapeptide induces panic-like attacks in healthy volunteers. Preliminary findings. Arch Gen Psychiatry 1989, 46:511-517.
24. DeSousa N.J., Wunderlich G.R., De Cabo C., Vaccarino F.J. The expression of behavioral sensitization to amphetamine: role of CCK(A) receptors. Pharmacol Biochem Behav 1999, 62:31-37.
25. Dornan W.A., Bloch G.J., Priest C.A., Micevych P.E. Microinjection of cholecystokinin into the medial preoptic nucleus facilitates lordosis behavior in the female rat. Physiol Behav 1989, 45:969-974.
26. Evans B.E., Bock M.G., Rittle K.E., DiPardo R.M., Whitter W.L., Veber D.F., et al. Design of potent, orally effective, nonpeptidal antagonists of the peptide hormone cholecystokinin. Proc Natl Acad Sci USA 1986, 83:4918-4922.
27. Fleming A.S., Kraemer G.W., Gonzalez A., Lovic V., Rees S., Melo A. Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharmacol Biochem Behav 2002, 73:61-75.
28. Funakoshi A., Miyasaka K., Shinozaki H., Masuda M., Kawanami T., Takata Y., et al. An animal model of congenital defect of gene expression of cholecystokinin (CCK)-A receptor. Biochem Biophys Res Commun 1995, 210:787-796.
29. Hadjiivanova C., Belcheva S., Belcheva I. Cholecystokinin and learning and memory processes. Acta Physiol Pharmacol Bulg 2003, 27:83-88.
30. Harhammer R., Schafer U., Henklein P., Ott T., Repke H. CCK-8-related C-terminal tetrapeptides: affinities for central CCKB and peripheral CCKA receptors. Eur J Pharmacol 1991, 209:263-266.
31. Harro J., Pold M., Vasar E. Anxiogenic-like action of caerulein, a CCK-8 receptor agonist, in the mouse: influence of acute and subchronic diazepam treatment. Naunyn Schmiedebergs Arch Pharmacol 1990, 341:62-67.
32. Harro J., Vasar E. Cholecystokinin-induced anxiety: how is it reflected in studies on exploratory behaviour?. Neurosci Biobehav Rev 1991, 15:473-477.
33. Hebb A.L., Poulin J.F., Roach S.P., Zacharko R.M., Drolet G. Cholecystokinin and endogenous opioid peptides: interactive influence on pain, cognition, and emotion. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1225-1238.
34. Hendrie C.A., Neill J.C., Shepherd J.K., Dourish C.T. The effects of CCKA and CCKB antagonists on activity in the black/white exploration model of anxiety in mice. Physiol Behav 1993, 54:689-693.
35. Higgins G.A., Sills T.L., Tomkins D.M., Sellers E.M., Vaccarino F.J. Evidence for the contribution of CCKB receptor mechanisms to individual differences in amphetamine-induced locomotion. Pharmacol Biochem Behav 1994, 48:1019-1024.
36. Hokfelt T., Rehfeld J.F., Skirboll L., Ivemark B., Goldstein M., Markey K. Evidence for coexistence of dopamine and CCK in meso-limbic neurones. Nature 1980, 285:476-478.
37. Hughes J., Boden P., Costall B., Domeney A., Kelly E., Horwell D.C., et al. Development of a class of selective cholecystokinin type B receptor antagonists having potent anxiolytic activity. Proc Natl Acad Sci USA 1990, 87:6728-6732.
38. Hurwitz I., Malkesman O., Stern Y., Schroeder M., Lavi-Avnon Y., Shayit M., et al. Stress and pain responses in rats lacking CCK1 receptors. Peptides 2006, 27:1483-1489.
39. Kobayashi M., Miyasaka K., Funakoshi A. Behavior abnormalities in the OLETF rats. Obesity and NIDDM: lessons from the OLETF rat 1999, Elsevier Science, Amsterdam. K. Shima (Ed.).
40. Kobayashi S., Ohta M., Miyasaka K., Funakoshi A. Decrease in exploratory behavior in naturally occurring cholecystokinin (CCK)-A receptor gene knockout rats. Neurosci Lett 1996, 214:61-64.
41. Lavi-Avnon Y., Malkesman O., Hurwitz I., Weller A. Mother-infant interactions in rats lacking CCK(A) receptors. Behav Neurosci 2004, 118:282-289.
42. Li X.L., Aou S., Hori T., Oomura Y. Spatial memory deficit and emotional abnormality in OLETF rats. Physiol Behav 2002, 75:15-23.
43. Little T.J., Horowitz M., Feinle-Bisset C. Role of cholecystokinin in appetite control and body weight regulation. Obes Rev 2005, 6:297-306.
44. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001, 24:1161-1192.
45. Miranda-Paiva C.M., Nasello A.G., Yim A.J., Felicio L.F. Puerperal blockade of cholecystokinin (CCK1) receptors disrupts maternal behavior in lactating rats. J Mol Neurosci 2002, 18:97-104.
46. Moran T.H., Schwartz G.J. Neurobiology of cholecystokinin. Crit Rev Neurobiol 1994, 9:1-28.
47. Nakamura H., Kihara Y., Tashiro M., Kanagawa K., Shirohara H., Yamamoto M., et al. Defects of cholecystokinin (CCK)-A receptor gene expression and CCK-A receptor-mediated biological functions in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. J Gastroenterol 1998, 33:702-709.
48. Peters J.H., Simasko S.M., Ritter R.C. Modulation of vagal afferent excitation and reduction of food intake by leptin and cholecystokinin. Physiol Behav 2006, 89:477-485.
49. Ravard S., Dourish C.T. Cholecystokinin and anxiety. Trends Pharmacol Sci 1990, 11:271-273.
50. Rotzinger S., Vaccarino F.J. Cholecystokinin receptor subtypes: role in the modulation of anxiety-related and reward-related behaviours in animal models. J Psychiatry Neurosci 2003, 28:171-181.
51. Schroeder M., Lavi-Avnon Y., Dagan M., Zagoory-Sharon O., Moran T.H., Weller A. Diurnal and nocturnal nursing behavior in the OLETF rat. Dev Psychobiol 2007, 49:323-333.
52. Schroeder M., Lavi-Avnon Y., Zagoory-Sharon O., Moran T.H., Weller A. Preobesity in the infant OLETF rat: the role of suckling. Dev Psychobiol 2007, 49:685-691.
53. Schroeder M., Schechter M., Fride E., Moran T.H., Weller A. Examining maternal influence on OLETF rats' early overweight: insights from a cross-fostering study. Dev Psychobiol 2009, 51:358-366.
54. Schroeder M., Zagoory-Sharon O., Lavi-Avnon Y., Moran T.H., Weller A. Weight gain and maternal behavior in CCK1 deficient rats. Physiol Behav 2006, 89:402-409.
55. Sei M., Sei H., Shima K. Spontaneous activity, sleep, and body temperature in rats lacking the CCK-A receptor. Physiol Behav 1999, 68:25-29.
56. Singh L., Field M.J., Hughes J., Menzies R., Oles R.J., Vass C.A., et al. The behavioural properties of CI-988, a selective cholecystokininB receptor antagonist. Br J Pharmacol 1991, 104:239-245.
57. Singh L., Lewis A.S., Field M.J., Hughes J., Woodruff G.N. Evidence for an involvement of the brain cholecystokinin B receptor in anxiety. Proc Natl Acad Sci USA 1991, 88:1130-1133.
58. Smith G.P. Cholecystokinin and treatment of meal size: proof of principle. Obesity (Silver Spring) 2006, 14(Suppl. 4):168S-170S.
59. Szelenyi Z. Cholecystokinin and thermoregulation-a minireview. Peptides 2001, 22:1245-1250.
60. van der Kooy D., Hunt S.P., Steinbusch H.W., Verhofstad A.A. Separate populations of cholecystokinin and 5-hydroxytryptamine-containing neuronal cells in the rat dorsal raphe, and their contribution to the ascending raphe projections. Neurosci Lett 1981, 26:25-30.
61. van Megen H.J., Westenberg H.G., den Boer J.A., Kahn R.S. Cholecystokinin in anxiety. Eur Neuropsychopharmacol 1996, 6:263-280.
62. Watanabe A., Okuno S., Okano M., Jordan S., Aihara K., Watanabe T.K., et al. Altered emotional behaviors in the diabetes mellitus OLETF type 1 congenic rat. Brain Res 2007, 1178:114-124.
63. Watanabe T.K., Suzuki M., Yamasaki Y., Okuno S., Hishigaki H., Ono T., et al. Mutated G-protein-coupled receptor GPR10 is responsible for the hyperphagia/dyslipidaemia/obesity locus of Dmo1 in the OLETF rat. Clin Exp Pharmacol Physiol 2005, 32:355-366.
64. Weller A. The ontogeny of postingestive inhibitory stimuli: examining the role of CCK. Dev Psychobiol 2006, 48:368-379.
65. Weller A., Gispan I.H. A cholecystokinin receptor antagonist blocks milk-induced but not maternal-contact-induced decrease in ultrasonic vocalization in rat pups. Dev Psychobiol 2000, 37:35-43.
66. Weller A., Gispan I.H., Armony-Sivan R., Ritter R.C., Smith G.P. Preloads of corn oil inhibit independent ingestion on postnatal day 15 in rats. Physiol Behav 1997, 62:871-874.
67. Weller A., Smith G.P., Gibbs J. Endogenous cholecystokinin reduces feeding in young rats. Science 1990, 247:1589-1591.
68. Weller A., Blass E.M. Behavioral evidence for cholecystokinin-opiate interactions in neonatal rats. Am J Physiol 1988, 255(6 Pt 2):R901-R907.
69. Wunderlich G.R., Rotzinger S., Bush D.E., DeSousa N.J., Vaccarino F.J. Cholecystokinin modulation of locomotor behavior in rats is sensitized by chronic amphetamine and chronic restraint stress exposure. Brain Res 2004, 1001:95-107.
70. Yamamoto Y., Akiyoshi J., Kiyota A., Katsuragi S., Tsutsumi T., Isogawa K., et al. Increased anxiety behavior in OLETF rats without cholecystokinin-A receptor. Brain Res Bull 2000, 53:789-792.