Functional expression of the norepinephrine transporter in cultured rat astrocytes

Journal of Neurochemistry

Volumn 84, Issue 1, 2003, Pages 136-144

  Inazu, Masato ^a   Takeda, Hiroshi ^a   Matsumiya, Teruhiko ^a  

^a TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Antidepressant; Astrocyte; Glia; Monoamine; Norepinephrine transporter

Indexed keywords

1 [2 (BENZHYDRYLOXY)ETHYL] 4 (3 PHENYLPROPYL)PIPERAZINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANTIDEPRESSANT AGENT; COCAINE; DESIPRAMINE; FLUVOXAMINE; MESSENGER RNA; MILNACIPRAN; NISOXETINE; NORADRENALIN TRANSPORTER; OUABAIN; POLYCLONAL ANTIBODY; SODIUM ION; VENLAFAXINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; ASTROCYTE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; GLIA CELL; IMMUNODETECTION; KINETICS; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NORADRENALIN UPTAKE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TARGET CELL; TEMPERATURE SENSITIVITY; TIME; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ENZYME INHIBITORS; MONOAMINE OXIDASE INHIBITORS; NA(+)-K(+)-EXCHANGING ATPASE; NOREPINEPHRINE; NOREPINEPHRINE PLASMA MEMBRANE TRANSPORT PROTEINS; OUABAIN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM; SYMPORTERS; TEMPERATURE; TIME FACTORS;

ANIMALIA; STROPHANTHUS GRATUS;

EID: 0037269322     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01514.x     Document Type: Article

References (69)

1. Apparsundaram S., Galli A., DeFelice L. J., Hartzell H. C. and Blakely R. D. (1998a) Acute regulation of norepinephrine transport: I. protein kinase C-linked muscarinic receptors influence transport capacity and transporter density in SK-N-SH cells. J. Pharmacol. Exp. Ther 287, 733-743.
2. Apparsundaram S., Schroeter S., Giovanetti E. and Blakely R. D. (1998b) Acute regulation of norepinephrine transport: II. PKC-modulated surface expression of human norepinephrine transporter proteins. J. Pharmacol. Exp. Ther. 287, 744-751.
3. Axelrod J., Whitby L. and Hertting G. (1961) Effect of psychotropic drugs on uptake. Science 133, 383-384.
4. Bel N., Figueras G., Vilaro M. T., Sunol C. and Artigas F. (1997) Antidepressant drugs inhibit a glial 5-hydroxytryptamine transporter in rat brain. Eur. J. Neurosci. 9, 1728-1738.
5. Blakely R. D., De Felice L. J. and Hartzell H. C. (1994) Molecular physiology of norepinephrine and serotonin transporters. J. Exp. Biol. 196, 263-281.
6. Bolden-Watson C. and Richelson E. (1993) Blockade by newly-developed antidepressants of biogenic amine uptake into rat brain synaptosomes. Life Sci. 52, 1023-1029.
7. Bönisch H. and Brüss M. (1994) The noradrenaline transporter of the neuronal plasma membrane. Ann. N. Y. Acad. Sci. 733, 193-202.
8. Bönisch H., Martiny-Baron G., Blum B. and Michael-Hepp J. (1990) Biochemical characterization and purification of the neuronal sodium-dependent noradrenaline transporter. J. Neural. Transm. Supplement 32, 413-419.
9. Bönisch H., Paulus G., Martiny-Baron G., Lingen B. and Coppeneur D. (1991) Molecular aspects of the neuronal noradrenaline transporter. J. Neural. Transm. Supplement 34, 11-17.
10. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
11. Brüss M., Hammermann R., Brimijoin S. and Bönisch H. (1995) Anti-peptide antibodies confirm the topology of the human norepinephrine transporter. J. Biol. Chem. 270, 9197-9201.
12. Brüss M., Pörzgen P., Bryan-Lluka L. J. and B̈nisch H. (1997) The rat norepinephrine transporter: molecular cloning from PC12 cells and functional expression. Brain Res. Mol. Brain Res. 52, 257-262.
13. Bryan-Lluka L. J., Westwood N. N. and O'Donnell S. R. (1992) Vascular uptake of catecholamines in perfused lungs of the rat occurs by the same process as Uptakel in noradrenergic neurones. Arch. Pharmacol. 345, 319-326.
14. Burton L. D., Kippenberger A. G., Lingen B., Brüss M., Bönisch H. and Christie D. L. (1998) A variant of the bovine noradrenaline transporter reveals the importance of the C-terminal region for correct targeting to the membrane and functional expression. Biochem. J. 330, 909-914.
15. Bzoskie L., Yen J., Tseng Y. T., Blount L., Kashiwai K. and Padbury J. F. (1997) Human placental norepinephrine transporter mRNA: expression and correlation with fetal condition at birth. Placenta 18, 205-210.
16. Carboni E., Tanda G. L., Frau R. and Di Chiara G. (1990) Blockade of the noradrenaline carrier increases extracellular dopamine concentrations in the prefrontal cortex: evidence that dopamine is taken up in vivo by noradrenergic terminals. J. Neurochem. 55, 1067-1070.
17. 50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108.
18. Chomczynski P. and Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
19. Cubells J. F., Kim K. S., Baker H., Volpe B. T., Chung Y., Houpt T. A., Wessel T. C. and Joh T. H. (1995) Differential in vivo regulation of mRNA encoding the norepinephrine transporter and tyrosine hydroxylase in rat adrenal medulla and locus ceruleus. J. Neurochem. 65, 502-509.
20. Di Chiara G., Tanda G. L., Frau R. and Carboni E. (1992) Heterologous monoamine reuptake: lack of transmitter specificity of neuron-specific carriers. Neurochem. Int. 20, 231S-235S.
21. Fitzgerald L. W., Kaplinsky L. and Kimelberg H. K. (1990) Serotonin metabolism by monoamine oxidase in rat primary astrocyte cultures. J. Neurochem. 55, 2008-2014.
22. Galli A., DeFelice L. J., Duke B. J., Moore K. R. and Blakely R. D. (1995) Sodium-dependent norepinephrine-induced currents in norepinephrine-transporter-transfected HEK-293 cells blocked by cocaine and antidepressants. J. Exp. Biol. 198, 2197-2212.
23. Gresch P. J., Sved A. F., Zigmond M. J. and Finlay J. M. (1995) Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J. Neurochem. 65, 111-116.
24. Griffith R. and Sutin J. (1996) Reactive astrocyte formation in vivo is regulated by noradrenergic axons. J. Comp. Neurol. 371, 362-375.
25. Hansson E. and Sellstrom A. (1983) MAO, COMT, and GABA-Tactivities in primary astroglial cultures. J. Neurochem. 40, 220-225.
26. 3H]5-HT uptake into glial plasmalemmal vesicles. Neurochem. Int. 33, 11-22.
27. Hoffman B. J., Hansson S. R., Mezey E. and Palkovits M. (1998) Localization and dynamic regulation of biogenic amine transporters in the mammalian central nervous system. Front. Neuroendocrinol. 19, 187-231.
28. 3H-serotonin by neurones and astrocytes in explant and primary cultures of rat CNS: effects of antidepressants. Int. J. Dev. Neurosci. 13, 897-908.
29. Inazu M., Kubota N., Takeda H., Zhang J., Kiuchi Y., Oguchi K. and Matsumiya T (1999a) Pharmacological characterization of dopamine transport in cultured rat astrocytes. Life Sci. 64, 2239-2245.
30. Inazu M., Takeda H., Ikoshi H., Uchida Y., Kubota N., Kiuchi Y., Oguchi K. and Matsumiya T (1999b) Regulation of dopamine uptake by basic fibroblast growth factor and epidermal growth factor in cultured rat astrocytes. Neurosci. Res. 34, 235-244.
31. Inazu M., Takeda H., Ikoshi H., Sugisawa M., Uchida Y. and Matsumiya T. (2001) Pharmacological characterization and visualization of the glial serotonin transporter. Neurochem. Int. 39, 39-49.
32. Iversen L. L. (1965) The inhibition of noradrenaline uptake by drugs. Adv. Drug Res. 2, 1-46.
33. 3H]norepinephrine by rat primary astrocyte cultures from neonatal rat cerebral cortex. Brain Res. 602, 41-44.
34. Kimelberg H. K. and Katz D. M. (1986) Regional differences in 5-hydroxytryptamine and catecholamine uptake in primary astrocyte cultures. J. Neurochem. 47, 1647-1652.
35. 3H]norepinephrine by primary astrocyte cultures and its inhibition by tricyclic antidepressants. J. Neurochem. 40, 1265-1270.
36. Kippenberger A. G., Palmer D. J., Comer A. M., Lipski J., Burton L. D. and Christie D. L. (1999) Localization of the noradrenaline transporter in rat adrenal medulla and PC12 cells: evidence for its ssociation with secretory granules in PC12 cells. J. Neurochem. 73, 1024-1032.
37. Kitayama S., Ikeda T., Mitsuhata C., Sato T., Morita K. and Dohi T. (1999) Dominant negative isoform of rat norepinephrine transporter produced by alternative RNA splicing. J. Biol. Chem. 274, 10731-10736.
38. Klimek V., Stockmeier C., Overholser J., Meltzer H. Y., Kalka S., Dilley G. and Ordway G. A. (1997) Reduced levels of norepinephrine transporters in the locus coeruleus in major depression. J. Neurosci. 17, 8451-8458.
39. Kubota N., Kiuchi Y., Nemoto M., Oyamada H., Ohno M., Funahashi H., Shioda S. and Oguchi K. (2001) Regulation of serotonin transporter gene expression in human glial cells by growth factors. Eur. J. Pharmacol. 417, 69-76.
40. Laming P. R., Kimelberg H., Robinson S., Salm A., Hawrylak N., Muller C., Roots B. and Ng K. (2000) Neuronal-glial interactions and behaviour. Neurosci. Biobehav. Rev. 24, 295-340.
41. Leconte I., Auzan C., Debant A., Rossi B. and Clauser E. (1992) N-linked oligosaccharide chains of the insulin receptor beta subunit are essential for transmembrane signaling. J. Biol. Chem. 267, 17415-17423.
42. Melikian H. E., McDonald J. K., Gu H., Rudnick G., Moore K. R. and Blakely R. D. (1994) Human norepinephrine transporter. Biosynthetic studies using a site-directed polyclonal antibody. J. Biol. Chem. 269, 12290-12297.
43. Melikian H. E., Ramamoorthy S., Tate C. G. and Blakely R. D. (1996) Inability to N-glycosylate the human norepinephrine transporter reduces protein stability, surface trafficking, and transport activity but not ligand recognition. Mol. Pharmacol. 50, 266-276.
44. Milner T. A., Lee A., Aicher S. A. and Rosin D. L. (1998) Hippocampal alpha2a-adrenergic receptors are located predominantly presynaptically but are also found postsynaptically and in selective astrocytes. J. Comp. Neurol. 395, 310-327.
45. Mochizuki D., Tsujita R., Yamada S., Kawasaki K., Otsuka Y., Hashimoto S., Hattori T., Kitamura Y. and Miki N. (2002) Neurochemical and behavioural characterization of milnacipran, a serotonin and noradrenaline reuptake inhibitor in rats. Psychopharmacology (Berl.) 162, 323-332.
46. Nguyen T. T. and Amara S. G. (1996) N-linked oligosaccharides are required for cell surface expression of the norepinephrine transporter but do not influence substrate or inhibitor recognition. J. Neurochem. 67, 645-655.
47. Ongur D., Drevets W. C. and Price J. L. (1998) Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc. Natl. Acad. Sci. USA 95, 13290-13295.
48. Paczkowski F. A., Bryan-Lluka L. J., Pörzgen P., Brüss M. and Bönisch H. (1999) Comparison of the pharmacological properties of cloned rat, human, and bovine norepinephrine transporters. J. Pharmacol. Exp. Ther. 290, 761-767.
49. Padbury J. F., Tseng Y. T., McGonnigal B., Penado K., Stephan M. and Rudnick G. (1997) Placental biogenic amine transporters: cloning and expression. Brain Res. Mol. Brain Res. 45, 163-168.
50. Pelton E. W., Kimelberg H. K., Shipherd S. V. and Bourke R. S. (1981) Dopamine and norepinephrine uptake and metabolism by astroglial cells in culture. Life Sci. 28, 1655-1663.
51. Pickel V. M. and Chan J. (2000) Ultrastructural localization of the serotonin transporter in limbic and motor compartments of the nucleus accumbens. J. Neurosci. 19, 7356-7366.
52. Povlock S. L. and Amara S. G. (1997) The structure and function of norepinephrine, dopamine, and serotonin transporters, in Neurotransmitter Transporters: Structure, Function, and Regulation (Reith M. E. A., ed.), pp. 1-28. Humana Press, Totowa, NJ.
53. Rajkowska G., Miguel-Hidalgo J. J., Wei J., Dilley G., Pittman S. D., Meltzer H. Y., Overholser J. C., Roth B. L. and Stockmeier C. A. (1999) Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol. Psychiatr. 45, 1085-1098.
54. Ramamoorthy S., Prasad P. D., Kulanthaivel P., Leibach F. H., Blakely R. D. and Ganapathy V. (1993) Expression of a cocaine-sensitive norepinephrine transporter in the human placental syncytiotrophoblast. Biochemistry 32, 1346-1353.
55. Ritz M. C., Lamb R. J., Goldberg S. R. and Kuhar M. J. (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237, 1219-1223.
56. Ronnett G. V., Knutson V. P., Kohanski R. A., Simpson T. L. and Lane M. D. (1984) Role of glycosylation in the processing of newly translated insulin proreceptor in 3T3-L1 adipocytes. J. Biol. Chem. 259, 4566-4575.
57. Rothman R. B., Lewis B., Dersch C., Xu H., Radesca L., de Costa B. R., Rice K. C., Kilburn R. B., Akunne H. C. and Pert A. (1993) Identification of a GBR12935 homolog, LR1111, which is over 4,000-fold selective for the dopamine transporter, relative to serotonin and norepinephrine transporters. Synapse 14, 34-39.
58. Schroeter S., Apparsundaram S., Wiley R. G., Miner L. H., Sesack S. R. and Blakely R. D. (2000) Immunolocalization of the cocaine- and antidepressant-sensitive I-norepinephrine transporter. J. Comp. Neurol. 420, 211-232.
59. Selemon L. D., Lidow M. S. and Goldman-Rakic P. S. (1999) Increased volume and glial density in primate prefrontal cortex associated with chronic antipsychotic drug exposure. Biol. Psychiatr. 46, 161-172.
60. Semenoff D. and Kimelberg H. K. (1985) Autoradiography of high affinity uptake of catecholamines by primary astrocyte cultures. Brain Res. 348, 125-136.
61. 3H]nisoxetine binding to norepinephrine uptake sites in olfactory bulb and frontal cortex of male rats. Synapse 31, 250-255.
62. Shimizu M., Nishida A., Zensho H. and Yamawaki S. (1996) Chronic antidepressant exposure enhances 5-hydroxytryptamine7 receptor-mediated cyclic adenosine monophosphate accumulation in rat frontocortical astrocytes. J. Pharmacol. Exp. Ther. 279, 1551-1558.
63. Tanda G., Carboni E., Frau R. and Di Chiara G. (1994) Increase of extracellular dopamine in the prefrontal cortex: a trait of drugs with antidepressant potential? Psychopharmacology (Berl.) 115, 285-288.
64. Tanda G., Pontieri F. E., Frau R. and Di Chiara G. (1997) Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine. Eur. J. Neurosci. 9, 2077-2085.
65. Tseng Y. T. and Padbury J. F. (1998) Expression of a pulmonary endothelial norepinephrine transporter. J. Neural. Transm. 105, 1187-1191.
66. Wayment H. K., Schenk J. O. and Sorg B. A. (2001) Characterization of extracellular dopamine clearance in the medial prefrontal cortex: role of monoamine uptake and monoamine oxidase inhibition. J. Neurosci. 21, 35-44.
67. 1A receptors to astroglial cells in adult rats: implications for neuronal-glial interactions and psychoactive drug mechanism of action. Synapse 14, 201-205.
68. Wilkin G. P., Marriott D. R., Cholewinski A. J., Wood J. N., Taylor G. W., Stephens G. J. and Djamgoz M. B. (1991) Receptor activation and its biochemical consequences in astrocytes. Ann. N. Y. Acad. Sci. 633, 475-488.
69. Yamamoto B. K. and Novotney S. (1998) Regulation of extracellular dopamine by the norepinephrine transporter. J. Neurochem. 71, 274-280.