Cannabinoids and gene expression during brain development

Neurotoxicity Research

Volumn 6, Issue 5, 2004, Pages 389-401

  Fernández Ruiz, Javier ^a   Gómez, María ^a   Hernández, Mariluz ^a   De Miguel, Rosario ^a   Ramos, José A ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

9 tetrahydrocannabinol; Brain; Cannabinoid receptors; Development; Endocannabinoids

Indexed keywords

CANNABINOID; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID;

BRAIN; BRAIN LEVEL; DRUG EFFECT; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PHYSIOLOGY; REVIEW;

BRAIN; BRAIN CHEMISTRY; CANNABINOIDS; ENDOCANNABINOIDS; GENE EXPRESSION; HUMANS; RECEPTOR, CANNABINOID, CB1;

EID: 16644392749     PISSN: 10298428     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF03033314     Document Type: Review

References (98)

1. Ashton CH (2001) Pharmacology and effects of cannabis: A brief review. Br. J. Psychiatr. 178, 101-106.
2. Azmitia EC (2001) Modern views on an ancient chemical: Serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res. Bull. 56, 413-424.
3. Behnke M and FD Eyler (1993) The consequences of prenatal substance use for the developing fetus, newborn, and young child. Int. J. Addict. 28, 1341-1391.
4. Berger B, C Verney, P Gaspar and A Febvret (1987) Transient expression of tyrosine hydroxylase immunoreactivity in some neurones of the rat neocortex during postnatal development. Dev. Brain Res. 23, 141-147.
5. Berrendero F, L García-Gil, ML Hernández, J Romero, M Cebeira, R de Miguel, JA Ramos and JJ Fernández-Ruiz (1998) Localization of mRNAexpression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development 125, 3179-3188.
6. Berrendero F, N Sepe, JA Ramos, V Di Marzo and JJ Fernández-Ruiz (1999) Análisis of cannabinoid receptor binding and mRNA expresión and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33, 181-191.
7. Bonnin A, R de Miguel, JC Rodríguez-Manzaneque, JJ Fernández-Ruiz, A Santos and JA Ramos (1994) Changes in tyrosine hydroxylase gene expression in mesencephalic catecholaminer-gic neurons of immature and adult male rats perinatally exposed to cannabinoids. Dev. Brain Res. 81, 147-150.
8. 9 -tetrahydro-cannabinol affects the gene expression and the activity of tyro-sine hydroxylase during early brain development. Life Sci. 56, 2177-2184.
9. 9 -tetrahydro-cannabinol on the fetal and early postnatal development of tyrosine hydroxylase-containing neurons in rat brain. J. Mol. Neurosci. 7, 291-308.
10. Bouaboula M, B Bourrie, M Rinaldi-Carmona, D Shire, G Le Fur and P Casellas (1995) Stimulation of cannabinoid receptor CB1 induces kros-24 expression in human astrocytoma cells. J. Biol. Chem. 270, 13973-13980.
11. Buckley NE, S Hansson, G Harta and E Mezey (1998) Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience 82, 1131-1149.
12. Burden-Galley SM, M Pendergast and V Lemmon (1997) The role of cell adhesion molecule L1 in axonal extension, growth cone motility, and signal transduction. Cell Tissue Res. 290, 415-422.
13. Burke RE (2003) Postnatal developmental programmed cell death in dopamine neurons. Ann. NY Acad. Sci. 991, 69-79.
14. Chan WY, DE Lorke, SC Tin and DT Yew (2002) Proliferation and apoptosis in the developing human neocortex. Anat. Rec. 267, 261-276.
15. 9 -tetrahydrocannabinol exposure reduces proenkephalin gene expression in the caudate-putamen of adult female rats. Life Sci. 63, 843-850.
16. Dahme M, U Bartsch, R Martini, B Anliker, M Schachner and N Mantei (1997) Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17, 346-349.
17. Dalterio SL (1986) Cannabinoid exposure: Effects on development. Neurobehav. Toxicol. Teratol. 8, 345-352.
18. Di Marzo V, A Fontana, H Cadas, S Schinelli, G Cimino, JC Schwartz and D Piomelli (1994) Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372, 686-691.
19. Emerit MB, M Riad and M Hamon (1992) Trophic effects of neu-rotransmitters during brain maturation. Biol. Neonate 62, 193-201.
20. Farlie PG, R Dringen, SM Rees, G Kannourakis and O Bernard (1995) Bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc. Natl. Acad. Sci. USA 92, 4397-4401.
21. Fernández-Ruiz JJ, F Rodríguez de Fonseca, M Navarro and JA Ramos (1992) Maternal cannabinoid exposure and brain development: changes in the ontogeny of dopaminergic neurons, In: Neurobiology and Neurophysiology of Cannabinoids, Biochemistry and Physiology of Substance Abuse, vol. IV, (Bartke A and LL Murphy, Eds.) (CRC Press, Boca Raton, FL), pp 119-164.
22. Fernández-Ruiz JJ, F Berrendero, ML Hernández, J Romero and JA Ramos (1999) Role of endocannabinoids in brain development. Life Sci. 65, 725-736.
23. Fernández-Ruiz JJ, F Berrendero, ML Hernández, J Romero and JA Ramos (2000) The endogenous cannabinoid system and brain development. Trends Neurosci. 23, 14-20.
24. Fride E (2002) Endocannabinoids in the central nervous system - an overview. Prostaglandins Leukot. Essent. Fatty Acids 66, 221-233.
25. 9-tetrahydrocannabinol in mice. Dev. Brain Res. 95, 131-134.
26. Fride E and E Shohami (2002) The endocannabinoid system: Function in survival of the embryo, the newborn and the neuron. NeuroReport 13, 1833-1841.
27. Fried PA and AM Smith (2001) Aliterature review of the consequences of prenatal marihuana exposure. An emerging theme of a deficiency in aspects of executive function. Neurotoxicol. Teratol. 23, 1-11.
28. 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.
29. 9 -tetrahydrocannabinol exposure did not alter dopamine transporter and tyrosine hydroxylase mRNAlev-els in midbrain dopaminergic neurons of adult male and females rats. Neurotoxicol. Teratol. 20, 549-553.
30. 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.
31. 9-tetrahydrocannabinol. Drug Alcohol Depend. 55, 127-136.
32. Gómez M, ML Hernández, B Johansson, R de Miguel, JA Ramos and J Fernández-Ruiz (2003) Prenatal cannabinoid exposure and gene expression for neural adhesion molecule L1 in the fetal rat brain. Dev. Brain Res. 147, 201-207.
33. 9-THC on operant morphine-reinforced behavior. Pharmacol. Biochem. Behav. 75, 577-584.
34. Gordon N (1995) Apoptosis (programmed cell death) and other reasons for elimination of neurons and axons. Brain Dev. 17, 73-77.
35. Guzmán M and C Sánchez (1999) Effects of cannabinoids on energy metabolism. Life Sci. 65, 657-664.
36. Guzmán M, C Sánchez and I Galve-Roperh (2001) Control of the cell survival/death decision by cannabinoids. J. Mol. Med. 78, 613-625.
37. Herkenham M, AB Lynn, MD Little, LS Melvin, MR Johnson, DR de Costa and KC Rice (1991a) Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. J. Neurosci. 11, 563-583.
38. Herkenham M, AB Lynn, BR de Costa and EK Richfield (1991b) Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res. 547, 267-264.
39. Hernández ML, L García-Gil, F Barrendero, JA Ramos and JJ Fernández-Ruiz (1997) Δ9-Tetrahydrocannabinol increases activity of tyrosine hydroxylase in cultured fetal mesencephalic neurons. J. Mol. Neurosci. 8, 83-91.
40. Hernández ML, F Berrendero, I Suárez, L García-Gil, M Cebeira, K Mackie, JA Ramos and J Fernández-Ruiz (2000) Cannabinoid CB1 receptors colocalize with tyrosine hydroxylase in cultured fetal mesencephalic neurons and their activation increases the levels of this enzyme. Brain Res. 857, 56-65.
41. Insel TR (1995) The development of brain and behaviour, In: Psychopharmacology: The Fourth Generation of Progress, (Bloom FE and DJ Kupfer, Eds.) (Raven Press), pp 683-694.
42. Itoh K, Y Sakurai, H Asou and M Umeda (2000) Differential expression of alternatevely spliced neural cell adhesion molecule L1 isoforms during oligodendrocyte maturation. J. Neurosci. Res. 60, 579-586.
43. Izumoto S, T Ohnishi, N Arita, S Hiraga, T Taki and T Hayakawa (1996) Gene expression of neural cell adhesion molecule L1 in malignant gliomas and biological significance of L1 in glioma invasion. Cancer Res. 56, 1440-1444.
44. Jacobson M (1993) Developmental Neurobiology (Plenum Press).
45. Jarskog LF and JH Gilmore (2000) Developmental expression of Bcl-2 protein in human cortex. Dev. Brain Res. 119, 225-230.
46. 9-tetrahydrocannabinol on the levels of opioid peptides, gonadotropin-releasing hormone and substance P in the adult male rat brain. Brain Res. 525, 78-83.
47. Lauder JM, J Liu, L Devaud and AL Morrow (1998) GABA as a trophic factor for developing monoamine neurons. Perspect. Dev. Neurobiol. 5, 247-259.
48. Leslie FM, Y Chen and UH Winzer-Serhan (1998) Opioid receptor and peptide mRNAexpression in proliferative zones of fetal rat central nervous system. Can. J. Physiol. Pharmacol. 76, 284-293.
49. Levitt P, JA Harvey, E Friedman, K Simansky and EH Murphy (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci. 20, 269-274.
50. Levitt P (1998) Prenatal effects of drugs of abuse on brain development. Drug Alcohol Depend. 51, 109-125.
51. Liljelund P, P Ghosh and AN van den Pol (1994) Expression of neural axon adshesion molecule L1 in the developing and adult rat brain. J. Biol. Chem. 269, 32886-32895.
52. Maccarrone M and A Finazzi-Agró (2003) The endocannabinoid system, anandamide and the regulation of mammalian cell apoptosis. Cell Death Differ. 10, 946-955.
53. Mailleux P and JJ Vanderhaeghen (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: A comparative receptor binding radioautography and in situ hybridization histochem-istry. Neuroscience 48, 655-668.
54. Manzanares J, J Corchero, J Romero, JJ Fernández-Ruiz, JA Ramos and JA Fuentes (1999) Pharmacological and biochemical interactions between opioids and cannabinoids. Trends Pharmacol. Sci. 20, 287-294.
55. Marshall CA, SO Suzuki and JE Goldman (2003) Gliogenic and neurogenic progenitors of the subventricular zone: Who are they, where did they come from, and where are they going? Glia 43, 52-61.
56. Martin LJ (2001) Neuronal death in nervous system development, disease, and injury. Int. J. Mol. Med. 7, 455-478.
57. Mato S, E Del Olmo and A Pazos (2003) Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur. J. Neurosci. 17, 1747-1754.
58. Mato S, E Del Olmo and A Pazos (2003) Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur. J. Neurosci. 17, 1747-1754.
59. Mereu G, M Fa, L Ferraro, R Cagiano, T Antonelli, M Tattoli, V Ghiglieri, S Tanganelli, GL Gessa and V Cuomo (2003) Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfuntion in hippocampal long-term potentiation and glutamate release. Proc. Natl. Acad. Sci. USA 100, 4915-4920.
60. Molina-Holgado E, JM Vela, A Arévalo-Martín, G Almazán, F Molina-Holgado, F Borrell and C Guaza (2002) Cannabinoids promote oligodendrocyte progenitor survival: Involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J. Neurosci. 22, 9742-9753.
61. 9-tetrahydrocannabinol on developing serotonergic system. Eur. J. Pharmacol. 316, 39-42.
62. 9-THC) alters indolamine levels and turnover in adult male and female rat brain regions. Brain Res. Bull. 43, 173-178.
63. Mooney SM and MW Miller (2001) Effects of prenatal exposure to ethanol on the expression of bcl-2, bax and caspase 3 in the developing rat cerebral cortex and thalamus. Brain Res. 911, 71-81.
64. Moos M, R Tacke, H Scherer, D Teplow, M Früh and M Schachner (1988) Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334, 701-703.
65. Murphy LL, RW Steger and A Bartke (1990) Psychoactive and non-psychoactive cannabinoids and their effects on reproductive neu-roendocrine parameters, In: Biochemistry and Physiology of Substance Abuse, vol. 2, (Watson RR, Ed.) (CRC Press, Boca Ratón, FL), pp 73-94.
66. Navarro M, F Rodríguez de Fonseca, ML Hernández, JA Ramos and JJ Fernández-Ruiz (1994) Motor behavior and nigrostriatal dopaminergic activity in adult rats perinatally exposed to cannabinoids. Pharmacol. Biochem. Behav. 47, 47-58.
67. Navarro M, R de Miguel, F Rodríguez de Fonseca, JA Ramos and JJ Fernández-Ruiz (1996) Perinatal cannabinoid exposure modifies the sociosexual approach behavior and the mesolimbic dopaminergic activity of adult male rats. Behav. Brain Res. 75, 91-98.
68. Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768-1771.
69. Panicker AK, M Bulusi, K Theleu and PF Maness (2003) Cellular signalling mechanisms of neural cell adhesion molecules. Front. Biosci. 8, 900-911.
70. Pendleton RG, A Rasheed, R Roychowdhury and R Hillman (1998) Anew role for catecholamines: Ontogenesis. Trends Pharmacol. Sci. 19, 248-251.
71. 9-tetrahydrocannabinol exposure modifies proenkephalin gene expression in the fetal rat brain: Sex dependent differences. Dev. Brain Res. 120, 77-81.
72. 9-tetrahydrocannabinol. Neurotoxicity Res. 4, 211-218.
73. Ramos JA, R de Miguel, M Cebeira, ML Hernández and J Fernández-Ruiz (2002) Exposure to cannabinoids in the development of endogenous cannabinoid system. Neurotoxicity Res. 4, 363-372.
74. Rodríguez de Fonseca F, M Cebeira, JJ Fernández-Ruiz, M Navarro and JA Ramos (1991) Effects of pre- and perinatal exposure to hashish extracts on the ontogeny of brain dopaminergic neurons. Neuroscience 43, 713-723.
75. Romero J, E García-Palomero, F Berrendero, L García-Gil, ML Hernández, JA Ramos and JJ Fernández-Ruiz (1997) Atypical location of cannabinoid receptors in white matter areas during rat brain development. Synapse 26, 317-323.
76. 9 -tetrahydrocannabinol in rats. Life Sci. 56, 2169-2176.
77. 9-tetrahydrocannabinol facilitates morphine-induced place conditioning in adult male offspring. Pharmacol. Biochem. Behav. 61, 229-238.
78. Rutledge SE, JW Chin and A Schepartz (2002) Aview to a kill: Lig-ands for Bcl-2 family proteins. Curr. Opin. Chem. Biol. 6, 479-485.
79. Saad B, D Constam, R Ortmann, M Moos, A Fontana and M Schanner (1991) Astrocyte-derived TGF-β 2 and NGF differentially regulate neural recognition molecule expression by cultured astrocytes. J. Cell Biol. 115, 473-484.
80. Sagan S, L Venance, Y Torrens, J Cordier, J Glowinski and C Giaume (1999) Anandamide and WIN 55212-2 inhibit cyclic AMP formation through G-protein-coupled receptors distinct from CB1 cannabinoid receptors in cultured astrocytes. Eur. J. Neurosci. 11, 691-699.
81. Sajovic P, E Kouvelas and E Trenkner (1986) Probable identity of NILE glycoprotein and the high-molecular-weight component of L1 antigen. J. Neurochem. 47, 541-546.
82. 9-Tetrahydrocannabinol stimulates glucose utilization in C6 glioma cells. Brain Res. 767, 64-71.
83. 9-Tetrahydrocannabinol induces apoptosis in C6 glioma cells. FEBS Lett. 436, 6-10.
84. Sánchez C, D Rueda, B Segui, I Galve-Roperh, T Levade and M Guzmán (2001) The CB1 cannabinoid receptor of astrocytes is coupled to sphingomyelin hydrolysis through the adaptor protein fan. Mol. Pharmacol. 59, 955-959.
85. Shivachar AC, BR Martín and EF Ellis (1996) Anandamide- and Δ9-tetrahydrocannabinol-evoked arachidonic acid mobilization and blockade by SR141716A[N-(Piperidin-1-yl)-5-(4-chlorophenyl)-1- (2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboximide hydrochloride]. Biochem. Pharmacol. 51, 669-676.
86. Specht LA, VM Pickel, TH Joh and DJ Reis (1981) Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J. Comp. Neurol. 199, 233-253.
87. Stallcup WB and L Beasley (1985) Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc. Natl. Acad. Sci. USA 82, 1276-1280.
88. Stiene-Martin A, PE Knapp, K Martin, JA Gurwell, S Ryan, SR Thornton, FL Smith and KF Hauser (2001) Opioid system diversity in developing neurons, astroglia, and oligodendroglia in the subventricular zone and striatum: Impact on gliogenesis in vivo. Glia 36, 78-88.
89. Sun F, S Akazawa, K Sugahara, S Kamihira, E Kawasaki, K Eguchi and T Koji (2002) Apoptosis in normal rat embryo tissues during early organogenesis: The possible involvement of Bax and Bcl-2. Arch. Histol. Cytol. 65, 145-157.
90. Tsou K, S Brown, MC Sañudo-Peña, K Mackie and JM Walker (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83, 393-411.
91. 9-THC) leads to changes in opioid-related behavioral patterns in rats. Brain Res. 680, 142-147.
92. 9-tetrahydrocannabinol facilitates morphine self-administration and changes μ opioid receptor binding in brain regions related to drug reinforcement in adult offspring female rats. Brain Res. 807, 101-109.
93. Venance L, D Piomelli, J Glowinski and C Giaume (1995) Inhibition of anandamide of gap junctions and intercellular calcium signalling in striatal astrocytes. Nature 376, 590-594.
94. Walters DE and LA Carr (1986) Changes in brain catecholamine mechanisms following perinatal exposure to marihuana. Pharmacol. Biochem. Behav. 25, 763-778.
95. Walters DE and LA Carr (1988) Perinatal exposure to cannabinoids alters neurochemical development in the rat brain. Pharmacol. Biochem. Behav. 29, 213-216.
96. Wang X, D Dow-Edwards, E Keller and YL Hurd (2003) Preferential limbic expression of the cannabinoid receptor mRNAin the human fetal brain. Neuroscience 118, 681-694.
97. Wong EV, S Kenwrick, P Willems and V Lemmon (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci. 18, 168-172.
98. Zimmermann KC, C Bonzon and DR Green (2001) The machinery of programmed cell death. Pharmacol. Ther. 92, 57-70.