Long-term behavioural and neuroendocrine effects of perinatal activation or blockade of CB1 cannabinoid receptors

Behavioural Pharmacology

Volumn 16, Issue 5-6, 2005, Pages 423-430

  Moreno, Margarita ^a   Escudero, L ^a   Munoz R ^a   Rodriguez De Fonseca, F ^a   Navarro, Miguel ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

9 tetrahydrocannabinol; Behaviour; Cannabinoid CB1 receptor; Corticosterone; Hormone secretion; Perinatal exposure; Rat; SR141716A

Indexed keywords

CANNABINOID 1 RECEPTOR; CORTICOSTERONE; CORTICOTROPIN; DRONABINOL; RIMONABANT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; EXPLORATORY BEHAVIOR; FEMALE; GESTATION PERIOD; HABITUATION; HORMONE RELEASE; IMMOBILIZATION; LACTATION; LOCOMOTION; MALE; NEUROENDOCRINOLOGY; NONHUMAN; ONTOGENY; PERINATAL DRUG EXPOSURE; PSYCHOMOTOR ACTIVITY; RAT; RECEPTOR BLOCKING; RECEPTOR UPREGULATION; SEX DIFFERENCE;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CORTICOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MALE; MOTOR ACTIVITY; PIPERIDINES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PYRAZOLES; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; SEX FACTORS; TETRAHYDROCANNABINOL; TIME FACTORS;

EID: 26044453633     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/00008877-200509000-00015     Document Type: Article

References (71)

1. Berrendero F, Sepe N, Ramos JA, Di Marzo V, Fernandez-Ruiz JJ (1999). Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33:181-191.
2. Bonnin A, De Miguel R, Rodriguez Manzaneque JC, Fernandez-Ruiz JJ, Santos A, Ramos JA (1994). Changes in tyrosine hydroxylase gene expression in mesencephalic catecholaminergic neurons of immature and adult male rats perinatally exposed to cannabinoids. Brain Res Dev Brain Res 81:147-153.
3. 9-tetrahydrocannabinol affects gene expression and the activity of tyrosine hydroxylase during early brain development. Life Sci 56:2177-2184.
4. 9-Tetrahydrocannabinol produces naloxone-blockade enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology (Berl) 102:156-162.
5. Del Arco I, Muñoz R, Rodriguez de Fonseca F, Escuredo L, Martin-Calderon JL, Navarro M, et al. (2000). Maternal exposure to the synthetic cannabinoid HU-210: effects on the endocrine and immune systems of the adult male offspring. Neuroimmunomodulation 7:16-26.
6. Demiere JM, Piazza PV, Guegan G, Abrous N, Maccari S, Le Moal M, et al. (1992). Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res 586:135-139.
7. Deroche V, Marinelli M, Maccari S, Le-Moal M, Simon H, Piazza PV (1995). Stress-induced sensitization and glucocorticoids. I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion. J Neurosci 15:7181-8100.
8. Di S, Malcher-Lopes R, Halmos KC, Tasker JG (2003). Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 23:4850-4857.
9. Femandez-Ruiz JJ, Rodriguez de Fonseca F, Navarro M, Ramos JA (1992). Maternal cannabinoid exposure and brain development: changes in the ontogeny of dopaminergic neurons. In: Bartke A, Murphy LL (editors): Neurobiology and Neurophysiology of Cannabinoids, Biochemistry and Physiology of Substance Abuse. Vol. IV. Boca Raton: CRC Press; pp. 119-164.
10. Fernandez-Ruiz JJ, Bonnin A, Cebeira M, Ramos JA (1994). Ontogenic and adult changes in the activity of hypothalamic and extrahypothalamic dopaminergic neurons after perinatal cannabinoid exposure in rats. In: Palomo T, Archer T (editors): Strategies for Studying Brain Disorders, vol. 1. England: Farrand Press; pp. 357-390.
11. Fernandez-Ruiz JJ, Muñoz RM, Romero J, Villanua MA, Makriyannis A, Ramos JA (1997). Time course of the effects of different cannabimimetics on prolactin and gonadotrophin secretion: evidence for the presence of CB-1 receptors in hypothalamic structures and their involvement in the effect of cannabimimetics. Biochem Pharmacol 53:1919-1927.
12. Fernandez-Ruiz JJ, Berrendero F, Hernandez ML, Ramos JA (2000). The endogenous cannabinoid system and brain development. Trends Neurosci 23:14-20.
13. Fride E (2004). The endocannabinoid-CB1 receptor system in pre- and postnatal life. Eur J Pharmacol 500:289-296.
14. Fride E, Mechoulam R (1996a). Developmental aspects of anandamide: ontogeny of response and prenatal exposure. Psychoneuroendocrinology 21: 157-172.
15. 9-tetrahydrocannabinol in mice. Brain Res Dev Brain Res 95:131-134.
16. Fried PA, Smith AM (2001). A literature review of the consequences of prenatal marihuana exposure. An emerging theme of a deficiency in aspects of executive function. Neurotoxicol Teratol 23:1-11.
17. Gamallo A, Alario P, Gonzalez-Abad MJ, Villanua MA (1992). Acute noise stress, ACTH administration and blood pressure alteration. Physiol Behav 51: 1201-1205.
18. Garcia-Gil L, De Miguel R, Ramos JA, Fernandez-Ruiz JJ (1996). Perinatal Delta-9-tetrahydrocannabinol exposure in rats modifies the responsiveness of midbrain dopaminergic neurons in adulthood to a variety of challenges with dopaminergic drugs. Drug Alcohol Depend 42:155-166.
19. Garcia-Gil L, De Miguel R, Romero J, Perez A, Ramos JA, Fernandez-Ruiz JJ (1999). Perinatal Delta-(9)-tetrahydrocannabinol exposure augmented the magnitude of motor inhibition caused by GABA(B), but not GABA(A), receptor agonists in adult rats. Neurotoxicol Teratol 21:277-283.
20. Gardner EL, Lowinson JM (1991). Marijuana's interaction with brain reward system: update. Pharmacol Biochem Behav 40:571-580.
21. Giuffrida A, Piomelli D (2000). The endocannabinoid system: a physiological perspective on its role in psychomotor control. Chem Phys Lipids 108: 151-158.
22. Gonzalez S, Bisogno T, Wenger T, Manzanares J, Milone A, Berrendero F, et al. (2000). Sex steroid influence on cannabinoid CB(1) receptor mRNA and endocannabinoid levels in the anterior pituitary gland. Biochem Biophys Res Commun 270:260-266.
23. Gueudet C, Santucci V, Rinaldi-Carmona M, Soubrie P, Le Fur G (1995). The CB1 cannabinoid receptor antagonist SR141716A affects A9 dopamine neuronal activity in the rat. Neuroreport 6:1421-1425.
24. Gurnack AM, Paul W (1997). Factors related to perinatal substance abuse in California County. Percept Mot Skills 84:1403-1408.
25. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, De Costa BR, et al. (1990). Cannabinoid receptor localization in the brain. Proc Natl Acad Sci USA 87:1932-1936.
26. Herkenham M, Lynn AB, Johnson MR, Melvin LS, De Costa BR, Rice EK (1991). Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
27. Ho BY, Stadnicka A, Prather PL, Buckley AR, Current LL, Bosnjak ZJ, et al. (2000). Cannabinoid CB1 receptor-mediated inhibition of prolactin release and signaling mechanisms in GH4C1 cells. Endocrinology 141:1675-1685.
28. Hutchings DE, Martin BR, Gamagaris Z, Miller N, Fico T (1989). Plasma concentrations of Delta-9-tetrahydrocannabinol in dams and fetuses following acute or multiple prenatal dosing in rats. Life Sci 44:697-701.
29. 14C-tetrahydrocannabinol to the mother. Eur J Pharmacol 22: 221-223.
30. Manzanares J, Corchero J, Fuentes JA (1999). Opioid and cannabinoid receptor-mediated regulation of the increase in adrenocorticotropin hormone and corticosterone plasma concentrations induced by central administration of Delta(9)-tetrahydrocannabinol in rats. Brain Res 839:173-179.
31. Marinelli M, Piazza PV (2002). Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16:387-394.
32. Martinez-Orgado J, Fernandez-Frutos B, Gonzalez R, Romero E, Uriguen L, Romero J, et al. (2003). Neuroprotection by the cannabinoid agonist WIN-55212 in an in vivo newborn rat model of acute severe asphyxia. Brain Res Mol Brain Res 114:132-139.
33. McCormick CM, Smythe JW, Sharma S, Meaney M (1995). Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res 84:55-61.
34. Mirmiran M, Brenner E, Van der Gugten J, Swaab DF (1985). Neurochemical and electrophysiological disturbances mediate developmental behavioural alterations produced by medicines. Neurobehav Toxicol Teratol 7:677.
35. 9-tetrahydrocannabinol increases presynaptic D2 receptor sensivity: a behavioural study in rats. Pharmacol Biochem Behav 75:565-575.
36. Murphy LL, Statham BC (1996). The role of cannabinoid receptors in the luteinizing hormone (LH) and adrenocorticotropin (ACTH) response to cannabinoids. Abstr Soc Neurosci 22:1344.
37. Murphy LL, Steger RW, Bartke A (1990a). Psychoactive and non psychoactive cannabinoids and their effects on reproductive neuroendocrine parameters. In: Watson RR (editor): Biochemistry and Physiology of Substance Abuse. Boca Raton: CRC; pp. 73-93.
38. Murphy LL, Steger RW, Smith MS, Bartke A (1990b). Effects of Delta-9-tetrahydrocannabinol, cannabinol, and cannabidiol, alone and in combinations, in luteinizing hormone and prolactin release and on hypothalamic neurotransmitters in the male rat. Neuroendocrinology 52:316-321.
39. Murphy LL, Muñoz RM, Adrian BA, Villanua MA (1998). Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion. Neurobiol Dis 5/6:432-446.
40. 9-tetrahydrocannabinol affects behavioral and neurochemical indices of mesolimbic dopaminergic activity. Behav Brain Res 5:37-46.
41. 9- tetrahydrocannabinol: possible involvement of nigrostriatal dopaminergic alterations. Pharmacol Biochem Behav 45:291-298.
42. Navarro M, Rodriguez de Fonseca F, Hernandez ML, Ramos JA, Fernandez-Ruiz JJ (1994a). Motor behavior and nigrostriatal dopaminergic activity in adult rats perinatally exposed to cannabinoids. Pharmacol Biochem Behav 47:47-58.
43. Navarro M, Rubio P, Rodriguez de Fonseca F (19946). Sex-dismorphic psychomotor activation after perinatal exposure to Delta-9-hydrocannabinol. An ontogenic study in Wistar rats. Psychopharmacology (Berl) 116: 414-422.
44. Navarro M, Rubio P, Rodriguez de Fonseca F (1995). Behavioral consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology (Berl) 122:1-14.
45. Navarro M, De Miguel R, Rodriguez de Fonseca F, Ramos JA, Fernandez-Ruiz JJ (1996). Perinatal cannabinoid exposure modifies sociosexual approach behavior and the mesolimbic dopaminergic activity of adult male rats. Behav Brain Res 75:91-98.
46. Paria BC, Dey SK (2000). Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation. Chem Phys Lipids 108:211-220.
47. Perio A, Rinaldi-Carmona M, Maruani J, Barth F, Le Fur G, Soubrie P (1996). Central mediation of the cannabinoid cue: activity of a selective CB1 antagonist SR141716A. Behav Pharmacol 7:65-71.
48. Piazza PV, Barrot M, Rouge-Pont F, Marinelli M, Maccari S, Abrous DN, et al. (1996a). Suppression of glucocorticoid secretion and antipsychotic drugs have similar effect on the mesolimbic dopaminergic trasmission. Proc Natl Acad Sci USA 93:15445-15450.
49. Piazza PV, Marinelli M, Rouge-Pont F, Deroche V, Maccari S, Simon H, et al. (1996b). Stress, glucocorticoids, and mesencephalic dopaminergic neurons: a pathophysiological chain determining vulnerability to psychostimulant abuse. NIDA Res Monogr 163:277-299.
50. Rodriguez de Fonseca F, Cebeira M, Fernandez-Ruiz JJ, Navarro M, Ramos JA (1991 a). Effects of pre and perinatal exposure to hashish extracts on the ontogeny of brain dopaminergic neurons. Neuroscience 43:713-723.
51. Rodriguez de Fonseca F, Fernandez-Ruiz JJ, Eldridge JC, Steger RW, Bartke A, Murphy LL (1991b). Effects of the exposure to Delta-9-tetrahydrocannabinol on the adrenal medullary function: evidence of an acute effect and development of tolerance in chronic treatments. Pharmacol Biochem Behav 40:593-598.
52. Rodriguez de Fonseca F, Hernandez ML, De Miguel R, Fernandez-Ruiz JJ, Ramos JA (1992a). Early changes in the development of dopaminergic neurotransmission after maternal exposure to cannabinoids. Pharmacol Biochem Behav 41:469-474.
53. 9-Tetrahydrocannabinol administration affects anterior pituitary, corticoadrenal and adrenomedullary functions in male rats. Neuroendocrinology 11:147-156.
54. Rodriguez de Fonseca F, Ramos JA, Bonnin A, Fernandez-Ruiz JJ (1993). Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport 4:135-138.
55. Rodriguez de Fonseca F, Cebeira M, Hernandez ML, Ramos JA, Martin M, Fernandez-Ruiz JJ (1994). Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle, and changes after gonadectomy and sex steroid replacement. Life Sci 54:159-170.
56. Rodriguez de Fonseca F, Carrera MRA, Navarro M, Koob GF, Weiss F (1997). Activation of corticotropin releasing factor in the limbic system during cannabinoid withdrawal. Science 276:2050-2054.
57. Romero J, Garcia-Palomero E, Berrendero F, Garcia-Gil L, Hernandez ML, Ramos JA, et al. (1997). A typical location of cannabinoid receptors in white matter areas during rat brain development. Synapse 26:317-323.
58. 9-tetrahydrocannabinol in rats: possible role of pituitary-adrenal axis. Life Sci 56:2169-2176.
59. Rubio P, Rodriguez de Fonseca F, Martin-Calderon JL, Del Arco I, Bartolome S, Villanua MA, et al. (1998). Maternal exposure to low doses of Delta9-tetrahydrocannabinol facilitates morphine-induced place conditioning in adult male offspring. Pharmacol Biochem Behav 61:229-238.
60. Schlicker E, Kathmann M (2001). Modulation of transminer release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565-572.
61. Schmid PC, Paria BC, Krebsbach RJ, Schmid HH, Dey SK (1997). Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation. Proc Natl Acad Sci USA 94:4188-4192.
62. Suarez I, Bodega G, Ramos JA, Fernandez-Ruiz JJ, Fernandez B (2000). Neuronal and astroglial response to pre and perinatal exposure to Delta-9-tetra-hydrocannabinol in the rat substantia nigra. Dev Neurosci 22:253-263.
63. Vallee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997). Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626-2636.
64. Van der Stelt M, Di Marzo V (2003). The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133-150.
65. Van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, et al. (2001). Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21:8765-8771.
66. Villanua MA, Gamallo A (1985). Radioimmunoanálisis de corticosterona para la valoración de la funcion adrenal en ratas como indice de estrés. Endocrinologia 32:213-217.
67. Walters DE, Carr LA (1986). Changes in brain catecholamine mechanisms following perinatal exposure to marihuana. Pharmacol Biochem Behav 25:763-778.
68. Walters DE, Carr LA (1988). Perinatal exposure to cannabinoids alters neurochemical development in the rat brain. Pharmacol Biochem Behav 29:213-216.
69. Wenger T, Croix D, Tramu G, Leonardelli J (1991). Prenatally administered Delta-9-tetrahydrocannabinol temporarily inhibits the developing hypothalamo-pituitary system in rats. Pharmacol Biochem Behav 40:599-602.
70. Wenger T, Fragkakis G, Giannikou P, Yiannikakis N (1997). The effects of prenatally administered endogenous cannabinoid on rat offspring. Pharmacol Biochem Behav 58:537-544.
71. Yang ZM, Paria BC, Dey SK (1996). Activation of brain-type cannabinoid receptors interferes with preimplantation mouse embryo development. Biol Reprod 55:756-761.