Dose- and sex-dependent effects of the neurotoxin 6-hydroxydopamine on the nigrostriatal dopaminergic pathway of adult rats: Differential actions of estrogen in males and females

Neuroscience

Volumn 116, Issue 1, 2003, Pages 213-222

  Murray, H E ^a   Pillai, A V ^a   Mcarthur, S R ^a   Razvi, N ^a   Datla, K P ^a   Dexter, D T ^a   Gillies, G E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

6 OHDA lesions; Neurodegeneration; Neuroprotection; Parkinson's disease; Sexual dimorphism; Steroid hormones

Indexed keywords

ANDROGEN; ANDROSTANOLONE; DOPAMINE; ESTRADIOL; ESTROGEN; NEUROTOXIN; OXIDOPAMINE;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; DEPLETION; DISEASE PREDISPOSITION; DOPAMINERGIC SYSTEM; DOSE RESPONSE; ESTROGEN ACTIVITY; ESTROGEN BLOOD LEVEL; ESTROGEN THERAPY; FEMALE; GONADECTOMY; MAINTENANCE DRUG DOSE; MALE; NERVE INJURY; NEUROPROTECTION; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OVARIECTOMY; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

ADRENERGIC AGENTS; ANIMALS; CASTRATION; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DIHYDROTESTOSTERONE; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; NEURAL PATHWAYS; NEURONS; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; SUBSTANTIA NIGRA; SYMPATHOLYTICS; TYROSINE 3-MONOOXYGENASE;

EID: 0037439055     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00578-X     Document Type: Article

References (63)

1. Alkayed N.J., Harukuni I., Kimes A.S., London E.D., Traystman R.J., Hurn P.D. Gender-linked brain injury in experimental stroke. Stroke. 29:1998;159-165 ; discussion 166.
2. Andersen S.L., Rutstein M., Benzo J.M., Hostetter J.C., Teicher M.H. Sex differences in dopamine receptor overproduction and elimination. Neuroreport. 8:1997;1495-1498.
3. Anglade P., Tsuji S., Javoy-Agid F., Agid Y., Hirsch E.C. Plasticity of nerve afferents to nigrostriatal neurons in Parkinson's disease. Ann Neurol. 37:1995;265-272.
4. Bannon M.J., Whitty C.J. Age-related and regional differences in dopamine transporter mRNA expression in human midbrain. Neurology. 48:1997;969-977.
5. Bazzett T.J., Becker J.B. Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding. Brain Res. 637:1994;163-172.
6. Becker J.B. Direct effect of 17 beta-estradiol on striatum sex differences in dopamine release . Synapse. 5:1990;157-164.
7. Becker J.B. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci Lett. 118:1990;169-171.
8. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav. 64:1999;803-812.
9. Behl C., Holsboer F. The female sex hormone oestrogen as a neuroprotectant. Trends Pharmacol Sci. 20:1999;441-444.
10. Beyer C. Estrogen and the developing mammalian brain. Anat Embryol (Berl). 199:1999;379-390.
11. Beyer C., Karolczak M. Estrogenic stimulation of neurite growth in midbrain dopaminergic neurons depends on cAMP/protein kinase A signalling. J Neurosci Res. 59:2000;107-116.
12. Brenner D.E., Kukull W.A., Stergachis A., van Belle G., Bowen J.D., McCormick W.C., Teri L., Larson E.B. Postmenopausal estrogen replacement therapy and the risk of Alzheimer's disease a population-based case-control study . Am J Epidemiol. 140:1994;262-267.
13. Carman L.S., Gage F.H., Shults C.W. Partial lesion of the substantia nigra relation between extent of lesion and rotational behavior . Brain Res. 553:1991;275-283.
14. Carmignac D.F., Gabrielsson B.G., Robinson I.C. Growth hormone binding protein in the rat effects of gonadal steroids . Endocrinology. 133:1993;2445-2452.
15. Castner S.A., Xiao L., Becker J.B. Sex differences in striatal dopamine in vivo microdialysis and behavioral studies . Brain Res. 610:1993;127-134.
16. Dexter D.T., Brooks D.J., Harding A.E., Burn D.J., Muller D.P., Goss-Sampson M.A., Jenner P.G., Marsden C.D. Nigrostriatal function in vitamin E deficiency clinical, experimental, and positron emission tomographic studies . Ann Neurol. 35:1994;298-303.
17. Disshon K.A., Dluzen D.E. Estrogen as a neuromodulator of MPTP-induced neurotoxicity effects upon striatal dopamine release . Brain Res. 764:1997;9-16.
18. Disshon K.A., Dluzen D.E. Estrogen reduces acute striatal dopamine responses in vivo to the neurotoxin MPP+ in female, but not male rats. Brain Res. 868:2000;95-104.
19. Dluzen D. Estrogen decreases corpus striatal neurotoxicity in response to 6-hydroxydopamine. Brain Res. 767:1997;340-344.
20. Dluzen D., Jain R., Liu B. Modulatory effects of testosterone on 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced neurotoxicity. J Neurochem. 62:1994;94-101.
21. Dluzen D.E., McDermott J.L., Anderson L.I. Tamoxifen diminishes methamphetamine-induced striatal dopamine depletion in intact female and male mice. J Neuroendocrinol. 13:2001;618-624.
22. Dluzen D.E., McDermott J.L., Liu B. Estrogen alters MPTP-induced neurotoxicity in female mice effects on striatal dopamine concentrations and release . J Neurochem. 66:1996;658-666.
23. Dluzen D.E., McDermott J.L., Liu B. Estrogen as a neuroprotectant against MPTP-induced neurotoxicity in C57/B1 mice. Neurotoxicol Teratol. 18:1996;603-606.
24. Dubal D.B., Kashon M.L., Pettigrew L.C., Ren J.M., Finklestein S.P., Rau S.W., Wise P.M. Estradiol protects against ischemic injury. J Cereb Blood Flow Metab. 18:1998;1253-1258.
25. Finkelstein D.I., Stanic D., Parish C.L., Tomas D., Dickson K., Horne M.K. Axonal sprouting following lesions of the rat substantia nigra. Neuroscience. 97:2000;99-112.
26. Fornaguera J., Carey R.J., Huston J.P., Schwarting R.K. Behavioral asymmetries and recovery in rats with different degrees of unilateral striatal dopamine depletion. Brain Res. 664:1994;178-188.
27. Gao X., Dluzen D.E. The effect of testosterone upon methamphetamine neurotoxicity of the nigrostriatal dopaminergic system. Brain Res. 892:2001;63-69.
28. Garcia-Segura L.M., Azcoitia I., DonCarlos L.L. Neuroprotection by estradiol. Prog Neurobiol. 63:2001;29-60.
29. Garris P.A., Walker Q.D., Wightman R.M. Dopamine release and uptake rates both decrease in the partially denervated striatum in proportion to the loss of dopamine terminals. Brain Res. 753:1997;225-234.
30. Grandbois M., Morissette M., Callier S., Di Paolo T. Ovarian steroids and raloxifene prevent MPTP-induced dopamine depletion in mice. Neuroreport. 11:2000;343-346.
31. Harris H.A., Bapat A.R., Gonder D.S., Frail D.E. The ligand binding profiles of estrogen receptors alpha and beta are species dependent. Steroids. 67:2002;379-384.
32. Henderson V.W., Paganini-Hill A., Miller B.L., Elble R.J., Reyes P.F., Shoupe D., McCleary C.A., Klein R.A., Hake A.M., Farlow M.R. Estrogen for Alzheimer's disease in women randomized, double-blind, placebo-controlled trial . Neurology. 54:2000;295-301.
33. Jonasson U., Jonasson B., Saldeen T. Middle-aged men a risk category regarding fatal poisoning due to dextropropoxyphene and alcohol in combination . Prev Med. 31:2000;103-106.
34. Konradi C., Kornhuber J., Sofic E., Heckers S., Riederer P., Beckmann H. Variations of monoamines and their metabolites in the human brain putamen. Brain Res. 579:1992;285-290.
35. Maggs J.L., Morgan P., Park B.K. The sexually differentiated metabolism of [6, 7-3H]17 beta-oestradiol in rats male-specific 15 alpha- and male-selective 16 alpha-hydroxylation and female-selective catechol formation . J Steroid Biochem Mol Biol. 42:1992;65-76.
36. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocrinol Rev. 20:1999;279-307.
37. Miller D.B., Ali S.F., O'Callaghan J.P., Laws S.C. The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann N Y Acad Sci. 844:1998;153-165.
38. Naftolin F., Leranth C., Horvath T.L., Garcia-Segura L.M. Potential neuronal mechanisms of estrogen actions in synaptogenesis and synaptic plasticity. Cell Mol Neurobiol. 16:1996;213-223.
39. Nordeen E.J., Nordeen K.W., Sengelaub D.R., Arnold A.P. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science. 229:1985;671-673.
40. Quinn N.P., Marsden C.D. Menstrual-related fluctuations in Parkinson's disease. Mov Disord. 1:1986;85-87.
41. Robinson T.E., Becker J.B., Presty S.K. Long-term facilitation of amphetamine-induced rotational behavior and striatal dopamine release produced by a single exposure to amphetamine sex differences . Brain Res. 253:1982;231-241.
42. Robinson T.E., Castaneda E., Whishaw I.Q. Compensatory changes in striatal dopamine neurons following recovery from injury induced by 6-OHDA or methamphetamine a review of evidence from microdialysis studies . Can J Psychol. 44:1990;253-275.
43. Roof R.L., Hall E.D. Gender differences in acute CNS trauma and stroke neuroprotective effects of estrogen and progesterone . J Neurotrauma. 17:2000;367-388.
44. Sandyk R. Estrogens and the pathophysiology of Parkinson's disease. Int J Neurosci. 45:1989;119-122.
45. Sawada H., Shimohama S. Neuroprotective effects of estradiol in mesencephalic dopaminergic neurons. Neurosci Biobehav Rev. 24:2000;143-147.
46. Scallet A.C. Estrogens neuroprotective or neurotoxic? Ann N Y Acad Sci. 890:1999;121-132.
47. Schrag A., Ben-Shlomo Y., Quinn N.P. Cross sectional prevalence survey of idiopathic Parkinson's disease and Parkinsonism in London. Br Med J. 321:2000;21-22.
48. Schwarting R.K., Huston J.P. The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog Neurobiol. 50:1996;275-331.
49. Session D.R., Pearlstone M.M., Jewelewicz R., Kelly A.C. Estrogens and Parkinson's disease. Med Hypotheses. 42:1994;280-282.
50. Simerly R.B. Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res Mol Brain Res. 6:1989;297-310.
51. Song D.D., Haber S.N. Striatal responses to partial dopaminergic lesion evidence for compensatory sprouting . J Neurosci. 20:2000;5102-5114.
52. Stein D.G. Brain damage, sex hormones and recovery a new role for progesterone and estrogen? Trends Neurosci. 24:2001;386-391.
53. Swerdlow R.H., Parker W.D. Jr, Currie L.J., Bennett Jr J.P., Harrison M.B., Trugman J.M., Wooten G.F. Gender ratio differences between Parkinson's disease patients and their affected relatives. Parkinsonism Related Disorders. 7:2001;129-133.
54. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci. 19:1999;5792-5801.
55. Wagner G.C., Tekirian T.L., Cheo C.T. Sexual differences in sensitivity to methamphetamine toxicity. J Neural Transm Gen Sect. 93:1993;67-70.
56. Walker Q.D., Rooney M.B., Wightman R.M., Kuhn C.M. Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience. 95:2000;1061-1070.
57. Watanabe Y., Littleton-Kearney M.T., Traystman R.J., Hurn P.D. Estrogen restores postischemic pial microvascular dilation. Am J Physiol Heart Circ Physiol. 281:2001;H155-160.
58. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Liu Y. Estrogens trophic and protective factors in the adult brain . Front Neuroendocrinol. 22:2001;33-66.
59. Wong D.F., Broussolle E.P., Wand G., Villemagne V., Dannals R.F., Links J.M., Zacur H.A., Harris J., Naidu S., Braestrup C., et al. In vivo measurement of dopamine receptors in human brain by positron emission tomography age and sex differences . Ann N Y Acad Sci. 515:1988;203-214.
60. Yu L., Liao P.C. Sexual differences and estrous cycle in methamphetamine-induced dopamine and serotonin depletions in the striatum of mice. J Neural Transm. 107:2000;419-427.
61. Yu Y.L., Wagner G.C. Influence of gonadal hormones on sexual differences in sensitivity to methamphetamine-induced neurotoxicity. J Neural Transm Park Dis Dement Sect. 8:1994;215-221.
62. Zhang Y.Q., Shi J., Rajakumar G., Day A.L., Simpkins J.W. Effects of gender and estradiol treatment on focal brain ischemia. Brain Res. 784:1998;321-324.
63. Zigmond M.J., Hastings T.G. Neurochemical responses to lesions of dopaminergic neurons implications for compensation and neuropathology . Adv Pharmacol. 42:1998;788-792.