Prenatal cannabinoid exposure down-regulates glutamate transporter expressions (GLAST and EAAC1) in the rat cerebellum

Developmental Neuroscience

Volumn 26, Issue 1, 2004, Pages 45-53

  Suarez I ^a   Bodega, G ^a   Rubio, M ^a   Fernandez Ruiz J J ^b   Ramos, J A ^b   Fernandez B ^b  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

9 tetrahydrocannabinol; Astroglia; Bergmann glial cells; Cannabinoids; EAAC1; GLAST; Glutamate transporters

Indexed keywords

CANNABIS; DRONABINOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GESTATIONAL AGE; GLIA CELL; MACROGLIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAT; WESTERN BLOTTING;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANIMALS, NEWBORN; CEREBELLUM; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 3; FEMALE; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PSYCHOTROPIC DRUGS; RATS; SYMPORTERS; TETRAHYDROCANNABINOL;

EID: 7544222031     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000080711     Document Type: Article

References (56)

1. Al-Hayani A, Davies SN (2000): Cannabinoid receptor mediated inhibition of excitatory synaptic transmission in the rat hippocampal slice is developmentally regulated. Br J Pharmacol 131:663-665.
2. Altman J (1982): Morphological development of the rat cerebellum and some of its mechanisms. Exp Brain Res Suppl 6:8-49.
3. Antonelli T, Tanganelli S, Tomasini MC, Finetti S, Trabace L, Steardo L, Sabino V, Carratu MR, Cuomo V, Ferraro L (2004): Long-term effects on cortical glutamate release induced by prenatal exposure to the cannabinoid receptor agonist (R)-(+)-[2,3-dihydro-5-methyl-3-(4-morpholinylmethyl)-pyrrolo[1,2,3-de]- 1,4-benzoxacin-6-yl]-1-naphthalenylmethanone: An in vivo microdialysis study in the awake rat. Neuroscience 124:367-375.
4. Bergles DE, Dzubay JA, Jahr CE (1997): Glutamate transporter currents in Bergmann glial cells follow the time course of extrasynaptic glutamate. Proc Natl Acad Sci USA 94:14821-14825.
5. Breivogel CS, Childers SR (1998): The functional neuroanatomy of brain cannabinoid receptors. Neurobiol Dis 5:417-431.
6. Chaudhry FA, Lehre KP, Danbolt NC, van Lookeren Campagne M, Ottersen OP, Storm-Mathisen (1995): Glutamate transporters in glial plasma membranes: Highly differentiated localization revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
7. Clark BA, Barbour B (1997): Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J Physiol 502:335-350.
8. Derouiche A, Rauen T (1995): Coincidence of L-glutamate/L-aspartate transporter (Glast) and glutamine synthetase (GS) immunoreactions in retinal glia: Evidence for coupling of GLAST and GS in transmitter clearance. J Neurosci Res 42:131-143.
9. Devau G, Plachez C, Puyal J, Pierrot N, Ventéo S, Raymond J (2003): Expression of glutamate transporters in the medial and lateral vestibular nuclei during rat postnatal development. Dev Neurosci 25:332-342.
10. Drepper J, Timmann D, Kolb FP, Diener HC (1999): Non-motor associative learning in patients with isolated degenerative cerebellar disease. Brain 122:87-97.
11. Dzubay JA, Jahr CE (1999): The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19:5265-5274.
12. Fernández Ruiz JJ, Rodríguez 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 (eds): Neurobiology and Neurophysiology of Cannabinoids, Biochemistry and Physiology of Substance Abuse. Boca Raton, CRC Press, vol IV, pp 119-164.
13. Fonnum F (1984): Glutamate: A neurotransmitter in mammalian brain. J Neurochem 42:1-11.
14. Fukaya M, Yamada K, Nagashima M, Tanaka K, Watanabe M (1999): Down-regulated expression of glutamate transporter GLAST in Purkinje cell-associated astrocytes of reeler and weaver mutant cerebella. Neurosci Res 34:165-175.
15. Furuta A, Rothstein JD, Martin LJ (1997): Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
16. Ginsberg SD, Martin LJ, Rothstein JD (1995): Regional deafferentation down-regulates subtypes of glutamate transporter proteins. J Neurochem 65:2800-2803.
17. Hajos N, Ledent C, Freund TF (2001): Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1-4.
18. Hein C, Horváth E, Kugler P (2001): Glutamate transporter expression in astrocytes of the rat dentate gyrus following lesion of the entorhinal cortex. Eur J Neurosci 13:1839-1848.
19. Hoffman AF, Lupica CR (2001): Direct actions of cannabinoids on synaptic transmission in the nucleus accumbens: A comparison with opioids. J Neurophysiol 85:72-83.
20. Huang ChC, Lo SW, Hsu KS (2001): Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532:731-748.
21. Kuwamura M, Morikawa T, Yamate J, Kato K, Kotani T, Sakuma S (2000): Glial pathology in development of cerebellar dysplasia in the hereditary cerebellar vermis defect (CVD) rat. Acta Neuropathol 99:305-309.
22. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC (1995): Differential expression of two glial glutamate transporters in the rat brain: Quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
23. Lévénès C, Daniel H, Soubrié P, Crépel F (1998): Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol 510:867-879.
24. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH (1997): New evidence for neurotransmitter influences on brain development. Trends Neurosci 20:269-274.
25. Levy LM, Lehre KP, Walaas SI, Storm-Mathisen J, Danbolt NC (1995): Down-regulation of glial glutamate transporters after glutamatergic denervation in the rat brain. Eur J Neurosci 7:2036-2041.
26. Llinás RR, Walton KD (1990): Cerebellum; in Sheperd GM (ed): The Synaptic Organization of the Brain. Oxford, Oxford University Press, pp 214.
27. McDonald JW, Johnston MV (1990): Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 15:41-70.
28. Mereu G, Fá M, Ferraro L, Cagiano R, Antonelli T, Tattoli M, Ghiglieri V, Tanganelli S, Gessa GL, Cuomo V (2003): Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal longterm potentiation and glutamate release. Proc Natl Acad Sci USA 100:4915-4920.
29. Morisset V, Urban L (2001): Cannabinoid-induced presynaptic inhibition of glutamatergic EPSCs in substantia gelatinosa neurons of the rat spinal cord. J Neurophysiol 86:40-48.
30. Newman EA (2003): New roles for astrocytes: Regulation of synaptic transmission. Trends Neurosci 26:536-542.
31. Palay SL, Chan-Palay V (1974): The neuroglial cells of the cerebellar cortex; in Cerebellar Cortex: Cytology and Organization. Berlin, Springer, pp 288-320.
32. Parsons LM, Bower JM, Gao JH, Xiong J, Li J, Fox PT (1997): Lateral cerebellar hemispheres actively support sensory acquisition and discrimination rather than motor control. Learn Mem 4:49-62.
33. Peghini P, Janzen J, Stoffel W (1997): Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16:3822-3832.
34. Pfrieger FW (2002): Role of glia in synapse development. Curr Opin Neurobiol 12:486-490.
35. Poitry-Yamate CL, Vutskits L, Rauen T (2002): Neuronal-induced and glutamate-dependent activation of glial glutamate transporter function. J Neurochem 82:987-997.
36. Rakic P (1971): Neuron-glia relationship during granule cell migration in developing cerebellar cortex: A Golgi and electronmicroscopic study in Macacus rhesus. J Comp Neurol 141:283-312.
37. Ramón y Cajal S (1911): Histologie du système nerveux de l'homme et des vertébrés. Paris, Maloine.
38. Rodríguez de Fonseca F, Cebeira M, 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.
39. Rodríguez 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.
40. Romero J, Berrendero F, Manzanares J, Perez A, Corchero J, Fuentes JA, Fernandez-Ruiz JJ, Ramos JA (1998): Time-course of the cannabinoid receptor down-regulation in the adult rat brain caused by repeated exposure to delta-9-tetrahydrocannabinol. Synapse 30:298-308.
41. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996): Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
42. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW (1994): Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
43. Schmitt A, Asan E, Puschel B, Kugler P (1997): Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: Non-radioactive in situ hybridization and comparative immunohistochemistry. J Neurosci 17:1-10.
44. Shiga T, Ichikawa M, Hirata Y (1983): A Golgi study of Bergmann glial cells in developing rat cerebellum. Anat Embryol 167:191-201.
45. Suárez I, Bodega G, Fernández B (2000): Modulation of glutamate transporters (GLAST, GLT-1 and EAAC1) in the rat cerebellum following portocaval anastomosis. Brain Res 859:293-302.
46. Suárez I, Bodega G, Fernández B (2002a): Glutamine synthetase in brain: Effect of ammonia. Neurochem Int 41:123-142.
47. 9-tetrahydrocannabinol administration during development. Dev Neurosci 24:300-312.
48. 9-tetrahydrocannabinol exposure. Cerebellum 3:66-74.
49. Szabo B, Wallmichrath I, Mathonia P, Pfreundtner C (2000): Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neuroscience 97:89-97.
50. Takahashi KA, Linden DJ (2000): Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83:1167-1180.
51. Thompson RF, Thompson JK, Kim JJ, Krupa DJ, Shinkman PG (1998): The nature of reinforcement in cerebellar learning. Neurobiol Learn Mem 70:150-176.
52. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1997): Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
53. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001): Control of synapse number by glia. Science 291:569-570.
54. Voutsinos-Porche B, Knott G, Tanaka K, Quairiaux C, Welker E, Bonvento G (2003): Glial glutamate transporters and maturation of the mouse somatosensory cortex. Cereb Cortex 13:1110-1121.
55. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa SI, Kawashima N, Hori S, Takimoto M, Wada K, Tanaka K (1998): Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988.
56. Yamada K, Fukaya M, Shibata T, Kurihara H, Tanaka K, Inoue Y, Watanabe M (2000): Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells. J Comp Neurol 418:106-120.