Gender differences on MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) neurotoxicity in C57BL/6 mice

Molecular and Cellular Endocrinology

Volumn 311, Issue 1-2, 2009, Pages 62-68

  Ookubo, Masanori ^a,c   Yokoyama, Hironori ^a   Kato, Hiroyuki ^b   Araki, Tsutomu ^a  

^a Graduate School of Pharmaceutical Sciences   (Japan)

^b INTERNATIONAL UNIVERSITY OF HEALTH AND WELFARE   (Japan)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Dopamine system; Dopamine transporter; Gender; Mice; Parkinson's disease; Western blot analysis

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 3,4 DIHYDROXYPHENYLACETIC ACID; DOPAMINE; DOPAMINE TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; HOMOVANILLIC ACID; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; C57BL 6 MOUSE; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; ROTAROD TEST; SEX DIFFERENCE; WESTERN BLOTTING;

3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; BLOTTING, WESTERN; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HOMOVANILLIC ACID; MALE; MICE; MOTOR ACTIVITY; MPTP POISONING; NEOSTRIATUM; NERVOUS SYSTEM; NEUROTOXINS; SEX CHARACTERISTICS; TYROSINE 3-MONOOXYGENASE;

EID: 69249216450     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.07.011     Document Type: Article

References (62)

1. Araki T., Kumagai T., Tanaka K., Matsubara M., Kato H., Itoyama Y., and Imai Y. Neuroprotective effect of riluzole in MPTP-treated mice. Brain Res. 918 (2001) 176-181
2. Benedetti M.D., Maraganore D.M., Bower J.H., McDonnell S.K., Peterson B.J., Ahlskog J.E., Schaid D.J., and Rocca W.A. Hysterectomy, menopause, and estrogen use preceding Parkinson's disease: an exploratory case-control study. Mov. Disord. 16 (2001) 830-837
3. Beyer C. Estrogen and the developing mammalian brain. Anat. Embryol. (Berl.) 5 (1999) 379-390
4. Bhatt S.D., and Dluzen D.E. Dopamine transporter function differences between male and female CD-1 mice. Brain Res. 1035 (2005) 188-195
5. Borland L.M., and Michael A.C. Voltammetric study of the control of striatal dopamine release by glutamate. J. Neurochem. 91 (2004) 220-229
6. Bringham D., Macrae I.M., and Carswell H.V. Detrimental effects of 17beta-oestradiol after permanent middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 25 (2005) 414-420
7. Callier S., Morissette M., Grandbois M., and Di Palo T. Stereospecific prevention by 17beta-estradiol of MPTP-induced dopamine depletion in mice. Synapse 37 (2000) 245-251
8. Carswell H.V., Bingham D., Wallace K., Nilsen M., Graham D.I., Dominiczak A.F., and Macrae I.M. Differential effects of 17beta-estradiol upon stroke damage in stroke prone and normotensive rats. J. Cereb. Blood Flow Metab. 24 (2004) 298-304
9. Ciesielska A., Joniec I., Kurkowska-Jastrzebska I., Przbylkowski A., Gromadzka G., Czlonkowska A., and Czlonkowski A. Influence of age and gender on cytokine expression in a murine model of Parkinson's disease. Neuroimmunomodulation 14 (2007) 255-265
10. D'Astous M., Morissette M., and Di Paolo T. Effect of estrogen receptor agonists treatment in MPTP mice: evidence of neuroprotection by an ERα agonist. Neuropharmacology 47 (2004) 1180-1188
11. Di Paolo T. Modulation of brain dopamine transmission by sex steroids. Rev. Neurosci. 5 (1994) 27-41
12. Diamond S.G., Markham C.H., Hoehn M.M., McDowell F.H., and Muenter M.D. An examination of male-female differences in progression and mortality of Parkinson's disease. Neurology 40 (1990) 763-766
13. Dluzen D.E., and McDermott I.L. Gender differences in neurotoxicity of the nigrostriatal system: implication for Parkinson's disease. J. Gend. Specif. Med. 3 (2000) 36-42
14. Dluzen D.E., Anderson L.I., and Pilati C.F. Methamphetamine-gonadal steroid hormonal interactions: effects upon acute toxicity and striatal dopamine concentrations. Neurotoxicol. Teratol. 24 (2002) 267-273
15. Dringen R., Gutterer J.M., and Hirrlinger J. Gultathione metabolism in brain. Metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur. J. Biochem. 267 (2000) 4912-4916
16. Dubal D.B., Zhu H., Yu J., Rau S.W., Shughrue P.J., Merchenthaler I., Kindy M.S., and Wise P.M. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1952-1957
17. Farr T.D., Carswell H.V.O., Gsell W., and Macrase I.M. Estrogen receptor beta Agonist diarylpropiolnitrile (DNP) does not mediate neuroprotection in a rat model of permanent focal ischemia. Brain Res. 1185 (2007) 275-282
18. Farr T.D., Carswell H.V.O., McCann D.J., Sato M., Bryant H.U., Dodge J.A., and Macrase I.M. The selective oestrogen receptor modulater, LY362321, is not neuroprotective in rat model of transient focal ischemia. J. Neuroendocrinol. 20 (2008) 366-374
19. Ferraz A.C., Xavier L.L., Hernandes S., Sulzbach M., Viola G.G., Anselmo-Franci J.A., Achaval M., and Cunha C.D. Failure of estrogen to protect the substantia nigra pars compacta of female rats from lesion induced by 6-hydroxydopamine. Brain. Res. 986 (2003) 200-205
20. Freyaldenhoven T.E., Cadet J.L., and Ali S.F. The dopamine-depleting effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in CD-1 mice are gender-dependent. Brain Res. 735 (1996) 232-238
21. Gallo F., Morale M.C., Spaima-Purrello V., Tirolo C., Testa N., Farinella Z., Avola R., Beaudet A., and Marchetti B. Basic fibroblast growth factor (bFGF) acts on both neurons and glia to mediate the neurotrophic effects of astrocytes on LHRH neurons in culture. Synapse 36 (2000) 233-253
22. Gibson C.L., Gray L.J., Murphy S.P., and Bath P.M. Estrogens and experimental ischemic stroke: a systematic review. J. Cereb. Blood Flow Metab. 26 (2006) 1103-1113
23. Giladi N., and Honigman S. Hormones and Parkinson's disease. Neurology 45 (1995) 1028-1029
24. Haaxma C.A., Bloem B.R., Borm G.F., Oyen W.J., Leenders K.L., Eshuis S., Booij J., Dluzen D.E., and Horstink M.W. Gender differences in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 78 (2007) 819-824
25. Heikkila R.E., Hess A., and Duvoisin R.C. Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyidine in mice. Science 224 (1984) 1451-1453
26. Hurn P.D., and Macrae I.M. Estrogen as a neuroprotection in stroke. J. Cereb. Blood Flow Metab. 20 (2000) 631-652
27. Jakowec M.W., and Petzinger G.M. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine- lesioned model of Parkinson's disease, with emphasis on mice and nonhuman primates. Comp. Med. 54 (2004) 497-513
28. Jones S.R., Gainetdinov R.R., Jaber M., Giros B., Wightman R.M., and Caron M.G. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 4029-4034
29. Kuikka J.T., Tiihonen J., Karhu J., Bergstrom K.A., and Rasanen P. Fractal analysis of striatal dopamine re-uptake sites. Eur. J. Nucl. Med. 24 (1999) 1085-1090
30. Kurosaki R., Muramatsu Y., Kato H., Watanabe Y., Imai Y., Itoyama Y., and Araki T. Effect of angiotensin-converting enzyme inhibitor perindopril on interneurons in MPTP-treated mice. Eur. Neuropsychopharmacol. 15 (2005) 57-67
31. Langston J.W., Ballard P., Terud J.W., and Irwin I. Chronic parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219 (1983) 979-980
32. Langston J.W., Langston E.B., and Irwin I. MPTP-induced parkinsonism in human and no-human primates-clinical and experimental aspects. Acta Neurol. Scand. Suppl. 100 (1984) 49-54
33. 123I]FP-CIT SPECT in healthy volunteers. Eur. J. Nucl. Med. 27 (2000) 867-869
34. Miller D.B., Ali S.Y., O'Callaghan J., and Laws S.C. The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann. N.Y. Acad. Sci. 844 (1998) 153-165
35. Miller G.M., Gainetdinov R.R., Levey A.I., and Caron M.G. Dopamine transporters and neuronal injury. Trends Pharmacol. Sci. 20 (1999) 424-429
36. Morale M.C., Serra P.A., L'episcopo F., Tirolo C., Caniglia S., Testa N., Gennuso F., Giaquinta G., Rocchitta G., Desole M.S., Miele E., and Marchetti B. Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138 (2006) 869-878
37. Morissette M., and Di Paolo T. Sex and estrous cycle variations of rat striatal dopamine uptake sites. Neuroendocrinology 58 (1993) 16-22
38. Morissette M., Jourdain S., Al Sweidi S., Menniti F.S., Ramirez A.D., and Di Paolo T. Role of estrogen receptors in neuroprotection by estradiol against MPTP toxicity. Neuropharmacology 52 (2007) 1509-1520
39. Mozley L.H., Gur R.C., Mozley P.D., and Gur R.E. Striatal dopamine transporters and cognitive functioning in healthy men and women. Am. J. Psychiatry 158 (2001) 1492-1499
40. Murray H.E., Pillai A.V., Mcarthur S.R., Razvi N., Datla K.P., Dexter D.T., and Gillies G.E. 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 116 (2003) 213-222
41. Murphy S.J., McCullough L.D., and Smith J.M. Stroke in the female: role of biological sex and estrogen. ILAR J. 45 (2004) 147-159
42. Nawashiro H., Brenner M., Fukui S., Shimada K., and Hallenbeck J.M. High susceptibility to cerebral ischemia in GFAP-null mice. J. Cereb. Blood Flow Metab. 20 (2000) 1040-1044
43. Ookubo M., Yokoyma M., Takagi S., Kato H., and Araki T. Effects of estrogens on striatal damage after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrine (MPTP) neurotoxicity in male and female mice. Mol. Cell. Endocrinol. 296 (2008) 87-93
44. Quesada A., and Micevych C.E. Estrogen interacts with the IGF-1 system to protect nigrostriatal dopamine and maintain motoric behavior after 6-hydroxydopamine lesions. J. Neurosci. Res. 75 (2004) 107-116
45. Ramirez A.D., Liu X., and Menniti F.S. Repeated estradiol treatment prevents MPTP-induced dopamine depletion in male mice. Neuroendocrinology 77 (2003) 223-231
46. Rivest R., Falardardeau P., and Di Paolo T. Brain dopamine transporter: gender differences and effect of chronic haloperidol. Brain Res. 692 (1995) 269-272
47. Rocca W.A., Bower J.H., Maraganore D.M., Ahlskog J.E., Grossardt B.R., de Andrade M., and Melton Iii J. Increased risk of parkinsonism in women who underwent oophorectomy before menopause. Neurology 103 (2008) 98-114
48. Rodriguez-Navarro J.A., Solano R.M., Casarejos M.J., Gomez A., Perucho J., de Yebenes J.G., and Mena M.A. Gender differences and estrogen effects in parkin null mice. J. Neurochem. 106 (2008) 2143-2157
49. Saunders-Pullman R., Gordon-Elliott J., Parides M., Fahn S., Saunders H.R., and Bressman S. The effect of estrogen replacement on early Parkinson's disease. Neurology 52 (1999) 1417-1421
50. Sedelis M., Hofele K., Auburger G.W., Morgan S., Huston J.P., and Schwarting K.W. MPTP susceptibility in the mouse: behavioral, neurokemical, and histological analysis of gender and strain differences. Behav. Genet. 30 (2000) 171-182
51. Session D.R., Pearlstone M.M., Jewelewicz R., and Kelly A.C. Estrogens and Parkinson's disease. Med. Hypotheses 42 (1994) 280-282
52. Smeyne R.J., and Jakson-Lewis L.V. The MPTP model of Parkinson's disease. Brain Res. Mol. Brain Res. 134 (2005) 57-66
53. Strijks E., Kremer J.A., and Horstink M.W. Effects of female sex steroids on Parkinson's disease in postmenopausal women. Clin. Neuropharmacol. 22 (1999) 93-97
54. Takagi S., Hayakawa N., Kimoto H., Kato H., and Araki T. Damage of oligodendrocytes in the striatum after MPTP neurotoxicity in mice. J. Neural Transm. 114 (2007) 1553-1557
55. Theodorsson A., and Theodorosson E. Estradiol increases brain lesions in the cortex and lateral striatum after transient occlusion of the middle cerebral artery in rats: no effect of ischemia on galanin in the stroke area but decreased levels in the hippocampus. Peptides 26 (2005) 2257-2264
56. Tsang K.L., Ho S.L., and Lo S.K. Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology 54 (2000) 2292-2298
57. Tripanichkul W., Sripanichkulchai K., and Finkelstein D.I. Estrogen down-regulates glial activation in male mice following 1-methyl-4-phenyl-1,2,3,6-tetrahydro-pyridine intoxication. Brain Res. 1084 (2006) 28-37
58. Watanabe Y., Kato H., and Araki T. Protective action of neuronal nitric oxide synthase inhibitor in the MPTP mouse model of Parkinson's disease. Metab. Brain Dis. 23 (2008) 51-69
59. Whyte J., Hart T., Vaccaro M., Grieb-Neff P., Risser A., Polamsky M., and Coslett H. Effects of methylphenidate on attentional deficits after traumatic brain injury: a multidimensional, randomized, controlled trial. Am. J. Physiol. Med. Rehabil. 83 (2004) 401-420
60. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., and Liu Y. Estrogens: tropic and protective factors in the adult brain. Front. Neuroendcrinol. 22 (2001) 33-66
61. Yabe H., Choudhury M.E., Kubo M., Nishikawa N., Nagai M., and Nomoto M. Zonisamide increases dopamine turnover in the striatum of mice and common marmosets treated with MPTP. J. Pharmacol. Sci. 110 (2009) 64-68
62. Yokoyama H., Takagi S., Watanabe Y., Kato H., and Araki T. Role of reactive nitrogen and reactive oxygen species against MPTP neurotoxicity in mice. J. Neural Transm. 115 (2008) 831-842