Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats

Psychoneuroendocrinology

Volumn 32, Issue 6, 2007, Pages 636-650

  Llorente, Ricardo ^a   Arranz, Lorena ^a   Marco, Eva María ^a   Moreno, Enrique ^a   Puerto, Marta ^a   Guaza, Carmen ^b   De la Fuente, Mónica ^a   Viveros, Maria Paz ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO CAJAL   (Spain)

Author keywords

Anxiety; Cannabinoid; Corticosterone; Depressive like behaviour; Immune response; Maternal deprivation; Rat; Sex differences

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID; CORTICOSTERONE; IODINE 125;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AXILLARY LYMPH NODE; BODY WEIGHT; CHEMOTAXIS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DRUG EFFECT; FEMALE; FORCED SWIMMING TEST; HORMONE BLOOD LEVEL; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MALE; MATERNAL DEPRIVATION; MAZE TEST; NEUROENDOCRINOLOGY; NEUROIMMUNOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; SCHIZOPHRENIA; SEX DIFFERENCE; SPLEEN; STRESS; THYMUS;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BENZOXAZINES; BODY WEIGHT; CANNABINOIDS; CORTICOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; INJECTIONS, SUBCUTANEOUS; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MORPHOLINES; NAPHTHALENES; NEUROIMMUNOMODULATION; RATS; RATS, WISTAR; SEXUAL MATURATION; SWIMMING; TIME FACTORS;

EID: 34347394152     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2007.04.002     Document Type: Article

References (87)

1. Adriani W., and Laviola G. Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav. Pharmacol. 15 (2004) 341-352
2. Andreatini R., and Bacellar L.F. The relationship between anxiety and depression in animal models: a study using the forced swimming test and elevated plus-maze. Braz. J. Med. Biol. 32 (1999) 1121-1126
3. Borcel E., Perez-Alvarez L., de Ceballos M.L., Ramirez B.G., Marco E.M., Fernandez B., Rubio M., Guaza C., and Viveros M.P. Functional responses to the cannabinoid agonist WIN 55,212-2 in neonatal rats of both genders: influence of weaning. Pharmacol. Biochem. Behav. 78 (2004) 593-602
4. Braga R.J., Petrides G., and Figueira I. Anxiety disorders in schizophrenia. Compr. Psychiatry 45 (2004) 460-468
5. Cabral G.A., and Staab A. Effects on the immune system. Handb. Exp. Pharmacol. 168 (2005) 385-423
6. Chan G.C., Hinds T.R., Impey S., and Storm D.R. Hippocampal neurotoxicity of Delta9-tetrahydrocannabinol. J. Neurosci. 18 (1998) 5322-5332
7. Charmandari E., Kino T., Souvatzoglou E., and Chrousos G.P. Pediatric stress: hormonal mediators and human development. Horm. Res. 59 (2003) 161-179
8. Charmandari E., Tsigos C., and Chrousos G. Endocrinology of the stress response. Annu. Rev. Physiol. 67 (2005) 259-284
9. Chen J., Lee C.T., Errico S., Deng X., Cadet J.L., and Freed W.J. Protective effects of Delta(9)-tetrahydrocannabinol against N-methyl-d-aspartate-induced AF5 cell death. Brain Res. Mol. Brain Res. 134 (2005) 215-225
10. Cosentino M., Fietta A., Caldiroli E., Marino F., Rispoli L., Comelli M., Lecchini S., and Frigo G. Assessment of lymphocyte subsets and neutrophil leukocyte function in chronic psychiatric patients on long-term drug therapy. Prog. Neuropsychopharmacol. Biol. Psychiatry 20 (1996) 1117-1129
11. Correa F., Mestre L., Molina-Holgado E., Arevalo-Martin A., Docagne F., Romero E., Molina-Holgado F., Borrell J., and Guaza C. The role of cannabinoid system on immune modulation: therapeutic implications on CNS inflammation. Mini Rev. Med. Chem. 5 (2005) 671-675
12. De la Fuente M., Carazo M., Correa R., and Del Río M. Changes in macrophage and lymphocyte functions in guinea pigs after different amount of vitamin E ingestion. Br. J. Nutr. 84 (2000) 25-29
13. De la Fuente M., Baeza I., Guayerbas N., Puerto M., Castillo C., Salazar V., Ariznavarreta C., and F-Tresguerres J.A. Changes with ageing in several leukocyte functions of male and female rats. Biogerontology 5 (2004) 389-400
14. Del Río M., Hernanz A., and De la Fuente M. Bombesin, gastrin-releasing peptide, and neuromedin C modulate murine lymphocyte proliferation through adherent accessory cells and activate protein kinase C. Peptides 15 (1994) 15-22
15. Ellenbroek B.A. Animal models in the genomic era: possibilities and limitations with special emphasis on schizophrenia. Behav. Pharmacol. 14 (2003) 409-417
16. Ellenbroek B.A., and Cools A.R. Maternal separation reduces latent inhibition in the conditioned taste aversion paradigm. Neurosci. Res. Commun. 17 (1995) 27-33
17. Ellenbroek B.A., and Cools A.R. Early maternal deprivation and prepulse inhibition: the role of the postdeprivation environment. Pharmacol. Biochem. Behav. 73 (2002) 177-184
18. Ellenbroek B.A., van den Kroonenberg P.T., and Cools A.R. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr. Res. 30 (1998) 251-260
19. Ellenbroek B.A., de Bruin N.M., van Den Kroonenburg P.T., van Luijtelaar E.L., and Cools A.R. The effects of early maternal deprivation on auditory information processing in adult Wistar rats. Biol. Psychiatry 55 (2004) 701-707
20. Ellenbroek B.A., Derks N., and Park H.J. Early maternal deprivation retards neurodevelopment in Wistar rats. Stress 8 (2005) 247-257
21. Eskandari F., and Sternberg E.M. Neural-immune interactions in health and disease. Ann. NY Acad. Sci. 966 (2002) 20-27
22. Fenton W.S. Comorbid conditions in schizophrenia. Curr. Opin. Psychiatr. 14 (2001) 17-23
23. Fernández-Ruiz J.J., Berrendero F., Hernández M.L., Romero J., and Ramos J.A. Role of endocannabinoids in brain development. Life Sci. 65 (1999) 725-736
24. Fernández-Ruiz J., Berrendero F., Hernández M.L., and Ramos J.A. The endogenous cannabinoid system and brain development. Trends Neurosci. 23 (2000) 14-20
25. Fernández-Ruiz J., Gomez M., Hernandez M., de Miguel R., and Ramos J.A. Cannabinoids and gene expression during brain development. Neurotox. Res. 6 (2004) 389-401
26. File S.E. Behavioral detection of anxiolytic action. In: Elliot J.M., Heal D.J., and Marsden C.A. (Eds). Experimental Approaches to Anxiety and Depression (1992), Wiley, New York 25-44
27. File S.E., and Wardill A.G. Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 44 (1975) 53-59
28. Friedman H., Newton C., and Klein T.W. Microbial infections, immunomodulation, and drugs of abuse. Clin. Microbiol. Rev. 16 (2003) 209-219
29. Gaillard R.C. Interaction between the hypothalamo-pituitary-adrenal axis and the immunological system. Ann. Endocrinol. (Paris) 62 (2001) 155-163
30. Green A.I., Canuso C.M., Brenner M.J., and Wojcik J.D. Detection and management of comorbidity in patients with schizophrenia. Psychiatr. Clin. North Am. 26 (2003) 115-139
31. Groër M.W., Hill J., Wilkinson J.E., and Stuart A. Effects of separation and separation with supplemental stroking in BALb/c infant mice. Biol. Res. Nurs. 3 (2002) 119-131
32. Heim C., and Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49 (2001) 1023-1039
33. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., and Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11 (1991) 563-583
34. Husum H., Termeer E., Mathe A.A., Bolwig T.G., and Ellenbroek B.A. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology 42 (2002) 798-806
35. Julian M.D., Martín A.B., Cuellar B., Rodriguez De Fonseca F., Navarro M., Moratalla R., and Garcia-Segura L.M. Neuroanatomical relationship between type 1 cannabinoid receptors and dopaminergic systems in the rat basal ganglia. Neuroscience 119 (2003) 309-318
36. Kendler K.S., Sheth K., Gardner C.O., and Prescott C.A. Childhood parental loss and risk for first-onset of major depression and alcohol dependence: the time-decay of risk and sex differences. Psychol. Med. 32 (2002) 1187-1194
37. Klein T.W., Newton C., Larsen K., Lu L., Perkins I., Nong L., and Friedman H. The cannabinoid system and immune modulation. J. Leukoc. Biol. 74 (2003) 486-496
38. Levine S. The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors. Ann. NY Acad. Sci. 746 (1994) 275-288
39. Lewis D.A., and Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci. 25 (2002) 409-432
40. Lipska B.K., and Weinberger D.R. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23 (2000) 223-239
41. Luo Y.D., Patel M.K., Wiederhold M.D., and Ou D.W. Effects of cannabinoids and cocaine on the mitogen-induced transformations of lymphocytes of human and mouse origins. Int. J. Immunopharmacol. 14 (1992) 49-56
42. Macrì S., and Laviola G. Single episode of maternal deprivation and adult depressive profile in mice: interaction with cannabinoid exposure during adolescence. Behav. Brain Res. 154 (2004) 231-238
43. Marchetti B., Morale M.C., Testa N., Tirolo C., Caniglia S., Amor S., Dijkstra C.D., and Barden N. Stress, the immune system and vulnerability to degenerative disorders of the central nervous system in transgenic mice expressing glucocorticoid receptor antisense RNA. Brain Res. Brain Res. Rev. 37 (2001) 259-272
44. Marco E.M., Llorente R., Moreno E., Biscaia J.M., Guaza C., and Viveros M.P. Adolescent exposure to nicotine modifies acute functional responses to cannabinoid agonists in rats. Behav. Brain Res. 172 (2006) 46-53
45. Marco E.M., Adriani W., Canese R., Podo F., Viveros M.P., and Laviola G. Enhancement of endocannabinoid signalling during adolescence: modulation of impulsivity and long-term consequences on metabolic brain parameters in early maternally deprived rats. Pharmacol. Biochem. Behav. 86 (2007) 334-345
46. Marek G., and Merchant K. Developing therapeutics for schizophrenia and other psychotic disorders. Neuro. Rx. 2 (2005) 579-589
47. Marsicano G., and Lutz B. Neuromodulatory functions of the endocannabinoid system. J. Endocrinol. Invest. 29 (2006) 27-46
48. Martínez-Orgado J., Fernández-Frutos B., González R., Romero E., Urigüen L., Romero J., and Viveros M.P. Neuroprotection by the cannabinoid agonist WIN-55212 in an in vivo newborn rat model of acute severe asphyxia. Mol. Brain Res. 114 (2003) 132-139
49. Massi P., Fuzio D., Viganò D., Sacerdote P., and Parolaro D. Relative involvement of cannabinoid CB1 and CB2 receptors in the delta-9-tetrahydrocannabinol-induced inhibition of natural killer activity. Eur. J. Pharmacol. 387 (2000) 343-347
50. Massi P., Vaccani A., and Parolaro D. Cannabinoids, immune system and cytokine network. Curr. Pharm. Des. 12 (2006) 3135-3146
51. Mato S., Chevaleyre V., Robbe D., Pazos A., Castillo P.E., and Manzoni O.J. A single in vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat. Neurosci. 7 (2004) 585-586
52. McLusky N.J., and Naftolin F. Sexual differentiation of the central nervous system. Science 211 (1981) 1294-1303
53. Moises H.W., Schindler L., Leroux M., and Kirchner H. Decreased production of interferon alpha and interferon gamma in leucocyte cultures of schizophrenic patients. Acta Psychiatr. Scand. 72 (1985) 45-50
54. Moore C.L., and Morelli G.A. Mother rats interact differently with male and female offspring. J. Comp. Physiol. Psychol. 93 (1979) 677-684
55. Morgan C., Kirkbride J., Leff J., Craig T., Hutchinson G., McKenzie K., Morgan K., Dazzan P., Doody G.A., Jones P., Murray R., and Fearon P. Parental separation, loss and psychosis in different ethnic groups: a case-control study. Psychol. Med. 37 (2007) 495-503
56. Muller N., Riedel M., Gruber R., Ackenheil M., and Schwarz M.J. The immune system and schizophrenia. An integrative view. Ann. NY Acad. Sci. 917 (2000) 456-467
57. Pellow S., Chopin P., File S.E., and Briley M. Validation of open:closed arms entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14 (1985) 149-167
58. Pérez-Alvarez L., Baeza I., Arranz L., Marco E.M., Borcel E., Guaza C., Viveros M.P., and De la Fuente M. Behavioral, endocrine and immunological characteristics of a murine model of premature aging. Dev. Comp. Immunol. 29 (2005) 965-976
59. Pertwee R.G., and Ross R.A. Cannabinoid receptors and their ligands. Prostaglandins Leukot. Essent. Fat. Acids 66 (2002) 101-121
60. Phillips L.J., McGorry P.D., Garner B., Thompson K.N., Pantelis C., Wood S.J., and Berger G. Stress, the hippocampus and the hypothalamic-pituitary-adrenal axis: implications for the development of psychotic disorders. Aust. NZ J. Psychiatry 40 (2006) 725-741
61. Porsolt R.D. Animal models of depression: utility for transgenic research. Rev. Neurosci. 11 (2000) 53-58
62. Pross S., Klein T., Newton C., and Friedman H. Differential effects of marijuana components on proliferation of spleen, lymph node and thymus cells in vitro. Int. J. Immunopharmacol. 9 (1987) 363-370
63. Pross S.H., Klein T.W., Newton C.A., Smith J., Widen R., and Friedman H. Differential suppression of T-cell subpopulations by THC (delta-9-tetrahydrocannabinol). Int. J. Immunopharmacol. 12 (1990) 539-544
64. Pross S.H., Nakano Y., McHugh S., Widen R., Klein T.W., and Friedman H. Contrasting effects of THC on adult murine lymph node and spleen cell populations stimulated with mitogen or anti-CD3 antibody. Immunopharmacol. Immunotoxicol. 14 (1992) 675-687
65. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., and Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol. Psychiatry 7 (2002) 609-616
66. Rodriguez De Fonseca F., Ramos J.A., Bonin A., and Fernández-Ruiz J.J. Presence of cannabinoid binding sites in the brain from early postnatal ages. NeuroReport 4 (1993) 135-138
67. Romero E.M., Fernández B., Sagredo O., Gomez N., Urigüen L., Guaza C., et al. Antinociceptive, behavioural and neuroendocrine effects of CP 55,940 in young rats. Dev. Brain Res. 136 (2002) 85-92
68. Ross R.G., Heinlein S., and Tregellas H. High rates of comorbidity are found in childhood-onset schizophrenia. Schizophr. Res. 88 (2006) 90-95
69. Rots N.Y., de Jong J., Workel J.O., Levine S., Cools A.R., and De Kloet E.R. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J. Neuroendocrinol. 8 (1996) 501-506
70. Sacerdote P., Massi P., Panerai A.E., and Parolaro D. In vivo and in vitro treatment with the synthetic cannabinoid CP-55,940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J. Neuroimmunol. 109 (2000) 155-163
71. Sarne Y., and Mechoulam R. Cannabinoids: between neuroprotection and neurotoxicity. Curr. Drug Targets CNS Neurol. Disord. 4 (2005) 677-684
72. Schwarz M.J., Chiang S., Muller N., and Ackenheil M. T-helper-1 and T-helper-2 responses in psychiatric disorders. Brain Behav. Immun. 15 (2001) 340-370
73. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24 (2000) 417-463
74. Strous R.D., and Shoenfeld Y. Schizophrenia, autoimmunity and immune system dysregulation: a comprehensive model updated and revisited. J. Autoimmun. 27 (2006) 71-80
75. Suchecki D., and Tufik S. Long-term effects of maternal deprivation on the corticosterone response to stress in rats. Am. J. Physiol. 273 (1997) R1332-R1338
76. Teunis M.A., Heijnen C.J., Sluyter F., Bakker J.M., Van Dam A.M., Hof M., Cools A.R., and Kavelaars A. Maternal deprivation of rat pups increases clinical symptoms of experimental autoimmune encephalomyelitis at adult age. J. Neuroimmunol. 133 (2002) 30-38
77. Thorsell A., Slawecki C.J., El Khoury A., Mathe A.A., and Ehlers C.L. The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rats. Pharmacol. Biochem. Behav. 83 (2006) 28-34
78. Viveros M.P., Hernández R., Martinez I., and González P. Effects of social isolation and crowding upon adrenocortical reactivity and behavior in the rat. Rev. Esp. Fisiol. 44 (1988) 315-322
79. Viveros M.P., Llorente R., Moreno E., and Marco E.M. Behavioural and neuroendocrine effects of cannabinoids in critical developmental periods. Behav. Pharmacol. 16 (2005) 353-362
80. Viveros M.P., Marco E.M., and File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol. Biochem. Behav. 81 (2005) 331-342
81. Viveros M.P., Marco E.M., and File S.E. Nicotine and cannabinoids: parallels, contrasts and interactions. Neurosci. Biobehav. Rev. 30 (2006) 1161-1181
82. Weinberger D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry 44 (1987) 660-669
83. Weiss S.M., Wadsworth G., Fletcher A., and Dourish C.T. Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety. Neurosci. Biobehav. Rev. 23 (1998) 265-271
84. Wenger T., Gerendai I., Fezza F., Gonzalez S., Bisogno T., Fernandez-Ruiz J., and DiMarzo V. The hypothalamic levels of the endocannabinoid, anandamide, peak immediately before the onset of puberty in female rats. Life Sci. 70 (2002) 1407-1414
85. Workel J.O., Oitzl M.S., Fluttert M., Lesscher H., Karssen A., and de Kloet E.R. Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of brown Norway rats from youth to senescence. J. Neuroendocrinol. 13 (2001) 569-580
86. Zhang L.X., Levine S., Dent G., Zhan Y., Xing G., Okimoto D., Kathleen Gordon M., Post R.M., and Smith M.A. Maternal deprivation increases cell death in the infant rat brain. Brain Res. Dev. Brain Res. 133 (2002) 1-11
87. Zhu S.W., Yee B.K., Nyffeler M., Winblad B., Feldon J., and Mohammed A.H. Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav. Brain Res. 169 (2006) 10-20