Oestrogen regulates the expression and function of dopamine transporters in astrocytes of the nigrostriatal system

Journal of Neuroendocrinology

Volumn 19, Issue 9, 2007, Pages 682-690

  Karakaya, S ^a   Kipp, M ^a   Beyer, Cordian ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Astroglia; Dopamine; Midbrain striatum; Monoamine transporter; Neuroprotection; Oestrogen

Indexed keywords

DOPAMINE TRANSPORTER; ESTRADIOL; ESTROGEN; FULVESTRANT; OCTAMER TRANSCRIPTION FACTOR 4; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL CULTURE; CELL FUNCTION; CELL LEVEL; CELL METABOLISM; CONTROLLED STUDY; ELIMINATION REACTION; MESENCEPHALON; MOUSE; NEWBORN; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CORPUS STRIATUM; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ESTROGENS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED BALB C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUBSTANTIA NIGRA;

EID: 34548554160     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2007.01575.x     Document Type: Article

References (67)

1. Chinta SJ, Andersen JK. Dopaminergic neurons. Int J Biochem Cell Biol 2005; 37: 942-946.
2. Perrone-Capano CP, di Porzio U. Genetic and epigenetic control of midbrain dopaminergic neuron development. Int J Dev Biol 2000; 44: 679-687.
3. Olanow CW. The role of dopamine agonist in the treatment of early Parkinson's disease. Neurology 2002; 58: S33-S41.
4. Gerfen CR, McGinty JF, Young WS. Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J Neurosci 1991; 11: 1016-1031.
5. Schmidt U, Pilgrim C, Beyer C. Differentiative effects of dopamine on striatal neurons involve stimulation of the cAMP/PKA pathway. Mol Cell Neurosci 1998; 11: 9-18.
6. Schmidt U, Beyer C, Oestreicher B, Reisert I, Schilling K, Pilgrim C. Activation of dopaminergic D1 receptors promotes morphogenesis of developing striatal neurons. Neuroscience 1996; 74: 453-460.
7. Hansson E, Sellstrom A. MAO COMT, and GABA-T activities in primary astroglial cultures. J Neurochem 1983; 40: 220-225.
8. Huang G, Dragan M, Freeman D, Wilson JX. Activation of catechol-O-methyltransferase in astrocytes stimulates homocysteine synthesis and export to neurons. Glia 2005; 51: 47-55.
9. Hitri A, Hurd YL, Wyatt RJ, Deutsch SI. Molecular, functional and biochemical characteristics of the dopamine transporter. regional differences and clinical relevance. Clin Neuropharmacol 1994; 17: 1-22.
10. Loder MK, Melikian HE. The dopamine transporter constitutively internalizes and recycles in a protein kinase C-regulated manner in stably transfected PC12 cell lines. J Cell Biol 2003; 278: 22168-22174.
11. Torres GE. The dopamine transporter proteome. J Neurochem 2006; 97: 3-10.
12. Torres GE, Gainetdinov RR, Caron MG. Plasma membrane monoamine transporters: Structure, regulation and function. Nat Rev Neurosci 2003; 4: 13-25.
13. Foster JD, Cervinski MA, Gorentla BK, Vaughan RA. Regulation of the dopamine transporter by phosphorylation. Handbook Exp Pharmacol 2006; 175: 197-214.
14. Jayanthi LD, Ramamoorthy S. Regulation of monoamine transporters: influence of psychostimulants and therapeutic antidepressants. AAPS J 2005; 7: E728-E738.
15. Gainetdinov RR, Fumagalli F, Wang YM, Jones SR, Levey AI, Miller GW, Caron MG. Increased MPTP neurotoxicity in vesicular monoamine transporter 2 heterozygote knockout mice. J Neurochem 1998; 70: 1973-1978.
16. Whitehead RE, Ferrer JV, Javitch JA, Justice JB. Reaction of oxidized dopamine with endogenous cysteine residues in the human dopamine transporter. J Neurochem 2001; 76: 1242-1251.
17. Riddle EL, Fleckstein AE, Hanson GR. Role of monoamine transporters in mediating psychostimulant effects. AAPS J 2005; 7: E847-E851.
18. Weihe E, Eiden LE. Chemical neuroanatomy of the vesicular amine transporters. FASEB J 2000; 14: 2435-2449.
19. Wang YM, Gainetdinov RR, Fumagalli F, Xu F, Jones SR, Bock CB, Miller GW, Wightman RM, Caron MG. Knockout of the in vesicular monoamine transporter 2 gene in neonatal death and supersensitivity to cocaine and amphetamine. Neuron 1997; 19: 1285-1296.
20. Gainetdinov RR, Jones SR, Fumagalli F, Wightman RM, Caron MG. Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis. Brain Res Rev 1998; 26: 148-153.
21. Fumagalli F, Gainetdinov RRF, Wang YM, Valenzano KJ, Miller GW, Caron MG. Increased metamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knockout mice. J Neurosci 1999; 19: 2424-2431.
22. Ahnert-Hilgert G, Holtje M, Pahner I, Winter B, Brunk I. Regulation of vesicular neurotransmitter transporters. Rev Physiol Biochem Pharmacol 2003; 150: 140-160.
23. Hoffman BJ, Hansson SR, Mezey E, Palkovits M. Localization of dynamic regulation of biogenic amine transporters in the mammalian central nervous system. Front Neuroendocrinol 1998; 19: 187-231.
24. Eisenhofer G. The role of neuronal and extra-neuronal plasma membrane transporters in the inactivation of peripheral catecholamines. Pharmacol Ther 2001; 91: 35-62.
25. Takeda H, Inazu M, Matsumiya T. Astroglial dopamine transport is mediated by norepinephrine transporter. Naunyn Schmiedebergs Arch Pharmacol 2002; 366: 620-623.
26. Storch A, Ludolph AC, Schwarz J. Dopamine transporter: Involvement in selective dopaminergic neurotoxicity and degeneration. J Neural Transm 2004; 111: 1267-1286.
27. Hirsch EC, Hoglinger G, Rousselet E, Breidert T, Parain K, Feger J, Ruberg M, Prigent A, Cohen-Salmon C, Launay JM. Animal models of Parkinson's disease in rodents induced by toxins: An update. J Neural Transm 2003; 65: 89-100.
28. Horstink MW, Strijks E, Dluzen DE. Estrogen and Parkinson's disease. Adv Neurol 2003; 91: 107-114.
29. Kipp M, Karakaya S, Pawlak J, Araujo-Wright G, Arnold S, Beyer C. Estrogen and the development and protection of nigrostriatal dopaminergic neurons: Concerted action of a multitude of signals, protective molecules, and growth factors. Front Neuroendocrinol 2006; 27: 376-390.
30. Veiga S, Garcia-Segura LM, Azcoitia I. The neuroprotective properties of sex steroids and neurosteroids. Rev Neurol 2004; 39: 1043-1051.
31. Ivanova T, Küppers E, Engele J, Beyer C. Estrogen stimulates brain-derived neurotrophic factor in embryonic mouse midbrain neurons through a membrane-mediated and calcium-dependent mechanism. J Neurosci Res 2001; 66: 221-230.
32. Ivanova T, Beyer C. Estrogen regulates tyrosine hydroxylase expression in the neonate mouse midbrain. J Neurobiol 2003; 54: 638-647.
33. Beyer C, Reisert I, Pilgrim C. Dopamine content and metabolism in mesencephalic and diencephalic cell cultures: Sex differences and effects of sex steroids. J Neurosci 1991; 11: 1325-1333.
34. Beyer C, Karolczak M. Estrogenic stimulation of neurite growth in midbrain dopaminergic neurons depends on cAMP/protein kinase A signalling. J Neurosci Res 2000; 59: 107-116.
35. Ivanova T, Mendez P, Garcia-Segura LM, Beyer C. Rapid stimulation of the PI3-kinase/Akt signalling pathway in developing midbrain neurones by oestrogen. J Neuroendocrinol 2002; 14: 73-79.
36. Pawlak J, Beyer C. Developmental expression of MNAR mRNA in the developing mouse brain. Cell Tissue Res 2005; 320: 545-549.
37. Pawlak J, Brito V, Küppers E, Beyer C. Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Mol Brain Res 2005; 138: 1-7.
38. Härtig S, Beyer C, Arnold S. Effect of hypoxia upon the transcription pattern of subunit isoforms and kinetics of cytochrome c oxidase in astrocytes and neurons. J Neurochem 2006; 99: 937-951.
39. Brito V, Beyer C, Küppers E. BDNF-dependent stimulation of dopamine D5 receptor expression in developing striatal astrocytes involves PI3-kinase signaling. Glia 2004; 46: 284-295.
40. Pawlak J, Karolczak M, Krust A, Chambon P, Beyer C. Estrogen receptor-alpha is associated with the plasma membrane of astrocytes and coupled to the MAP/Src-kinase pathway. Glia 2005; 50: 270-275.
41. Semenoff D, Kimelberg HK. Autoradiography of high affinity uptake of catecholamines by primary astrocytes. Brain Res 1985; 348: 125-136.
42. Bosse R, Rivest R, Di Paolo T. Ovariectomy and estradiol treatment affect the dopamine transporter and its gene expression in the rat brain. Mol Brain Res 1997; 46: 343-346.
43. Watson CS, Alyea RA, Hawkins BE, Thomas ML, Cunningham KA, Jakubas AA. Estradiol effects on the dopamine transporter -protein levels, subcellular location, and function. J Mol Signal 2006; 1: 1-14.
44. McEwen BS. Estrogen actions throughout the brain. Recent Prog Horm Res 2002; 57: 357-384.
45. Mukai H, Tsurugizawa T, Ogiue-Ikeda M, Murakami G, Hojo Y, Ishii H, Kimoto T, Kawato S. Local neurosteroid production in the hippocampus. influence on synaptic plasticity of memory. Neuroendocrinology 2006; 84: 255-263.
46. Le Saux M, Di Paolo T. Influence of oestrogenic compounds on monoamine transporters in rat striatum. J Neuroendocrinol 2006; 18: 25-32.
47. Gardiner SA, Morrison MF, Mozley PD, Mozley LH, Brensinger C, Bilker W, Newberg A, Battistini M. Pilot study on the effect of estrogen replacement therapy on brain dopamine transporter availability in healthy, postmenopausal women. Am J Geriatr Psychiatry 2004; 12: 621-630.
48. Datla KP, Murray HE, Pillai AV, Gillies GE, Dexter DT. Differences in dopaminergic neuroprotective effects of estrogen during estrous cycle. Neuroreport 2003; 14: 47-50.
49. McArthur S, Murray HE, Dhankot A, Dexter DT, Gillies GE. Striatal susceptibility to a dopaminergic neurotoxin is independent of sex hormone effects on cell survival and DAT expression but is exacerbated by central aromatase inhibition. J Neurochem 2007; 100: 678-692.
50. Gillies GE, Murray HE, Dexter D, McArthur S. Sex dimorphisms in the neuroprotective effects of estrogen in an animal model of Parkinson's disease. Pharmacol Biochem Behav 2004; 78: 513-522.
51. Shulman LM, Bhat V. Gender disparities in Parkinson's disease. Expert Rev Neurother 2006; 6: 407-416.
52. Saunders-Pullmann R. Estrogens and Parkinson's disease: Neuroprotective, symptomatic, neither, or both? Endocrine 2003; 21: 81-87.
53. Kajta M, Beyer C. Cellular strategies of estrogen-mediated neuroprotection during brain development. Endocrine 2003; 21: 3-9.
54. Behl C. Estrogen as a neuroprotective hormone. Nat Rev Neurosci 2002; 3: 433-422.
55. Dluzen DE. Unconventional effects of estrogen uncovered. Trends Pharmacol Sci 2005; 26: 485-487.
56. Henderson VW. Oestrogen and dementia. Novartis Foundation Symp 2000; 230: 254-273.
57. Kenchappa RS, Diwakar L, Annepu J, Ravindranath V. Estrogen and neuroprotection: Higher constitutive expression of glutredoxin in female mice offers protection against MPTP-mediated neuroprotection. FASEB J 2004; 18: 1102-1104.
58. Xu HX, Gouras GK, Greenfield JP, Nincent B, Naslund J, Mazzarelli L, Fried G, Jovanovic JN, Seeger M, Relkin NR, Liao F, Checler F, Buxbaum JD, Chait BT, Tinakaran G, Sisodia SS, Wang R, Greengard P, Gandy S. Estrogen reduces neuronal generation of Alzheimer β-amyloid peptides. Nat Med 1998; 4: 447-451.
59. Kritzer MF. Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral field in the rat. J Comp Neurol 1997; 379: 247-260.
60. Kueppers E, Beyer C. Expression of estrogen receptor-alpha and beta mRNA in the developing and adult mouse striatum. Neurosci Lett 1999; 276: 95-98.
61. Leranth C, Roth RH, Elsworth JD, Naftolin F, Horvath TL. Redmond DE. Estrogen is essential for maintaining nigrostriatal neurons in primates: implications for Parkinson's disease and memory. J Neurosci 2000; 20: 8604-8609.
62. D'Astous M, Morissette M, Di Paolo T. Effect of estrogen receptor agonist treatment in MPTP mice: Evidence of neuroprotection by an ER alpha agonist. Neuropharmacology 2004; 47: 1180-1188.
63. Morale MC, Serra PA, L'episcopo F, Tirolo C, Caniglia S, Testa N, Gennuso F, Giaquinta G, Rocchitta G, Desole MS, Miele E, Marchetti B. Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. 2006; 138: 869-878.
64. Gajjar TM, Anderson LI. Dluzen DE. Acute effects of estrogen upon methamphetamine induced neurotoxicity of the nigrostriatal dopaminergic system. J Neural Transm 2003; 110: 1215-1224.
65. Currie LJ, Harrison MB, Trugman JM, Bennett JP, Wooten GF. Postmenopausal estrogen use affects risk for Parkinson's disease. Arch Neurol 2004; 61: 886-888.
66. Jourdain S, Morissette M, Morin N, Di Paolo T. Oestrogens prevent loss of dopamine transporter (DAT) and vesicular monoamine transporter (VMAT2) in substantia nigra of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice. J Neuroendocrinol 2005; 17: 509-517.
67. Beckstead MJ, Grandy DK, Wickman K, Williams JT. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004; 42: 939-946.