Sex differences in Parkinson's disease and other movement disorders

Experimental Neurology

Volumn 259, Issue , 2014, Pages 44-56

  Smith, Kara M ^a   Dahodwala, Nabila ^a  

^a Parkinson's Disease and Movement Disorders Center   (United States)

Author keywords

Chorea; Estrogen; Huntington's disease; Neuroprotection; Parkinson's disease; Sex chromosome; Sex differences; Testosterone; Tics; Tourette's syndrome

Indexed keywords

CAFFEINE; ESTROGEN; ESTROGEN RECEPTOR; PRASTERONE; PROGESTERONE; TESTOSTERONE; ANDROGEN; DOPAMINE; NEUROPROTECTIVE AGENT;

BASAL GANGLION; CHOREA MINOR; CLINICAL STUDY; DOPAMINERGIC ACTIVITY; DOWN REGULATION; GILLES DE LA TOURETTE SYNDROME; HUMAN; HUNTINGTON CHOREA; MOLECULAR INTERACTION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SEX DIFFERENCE; X CHROMOSOME; Y CHROMOSOME; ANIMAL; CHOREA; DRUG EFFECT; FEMALE; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; SEX CHROMOSOME; SEX DIFFERENCES; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; TIC;

CHOREA; ESTROGEN; HUNTINGTON'S DISEASE; NEUROPROTECTION; PARKINSON'S DISEASE; SEX CHROMOSOME; SEX DIFFERENCES; TESTOSTERONE; TICS; TOURETTE'S SYNDROME;

ANDROGENS; ANIMALS; CAFFEINE; CHOREA GRAVIDARUM; DOPAMINE; ESTROGENS; FEMALE; HUMANS; HUNTINGTON DISEASE; MALE; MOVEMENT DISORDERS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; PROGESTERONE; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TICS; TOURETTE SYNDROME;

EID: 84907288454     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.03.010     Document Type: Review

References (115)

1. Al-Sweidi, S., Morissette, M., Bourque, M., Di Paolo, T., Estrogen receptors and gonadal steroids in vulnerability and protection of dopamine neurons in a mouse model of Parkinson's disease. Neuropharmacology 61 (2011), 583–591.
2. Anderson, L.I., Leipheimer, R.E., Dluzen, D.E., Effects of neonatal and prepubertal hormonal manipulations upon estrogen neuroprotection of the nigrostriatal dopaminergic system within female and male mice. Neuroscience 130 (2005), 369–382.
3. Anon, A randomized pilot trial of estrogen replacement therapy in post-menopausal women with Parkinson's disease. Parkinsonism Relat. Disord. 17 (2011), 757–760.
4. Arvin, M., Fedorkova, L., Disshon, K.A., Dluzen, D.E., Leipheimer, R.E., Estrogen modulates responses of striatal dopamine neurons to MPP(+): evaluations using in vitro and in vivo techniques. Brain Res 872 (2000), 160–171.
5. Ascherio, A., Prospective study of caffeine consumption and risk of Parkinson's disease in men and women. Ann. Neurol., 2001, 1–8.
6. Ascherio, A., Coffee consumption, gender, and Parkinson's disease mortality in the Cancer Prevention Study II Cohort: the modifying effects of estrogen. Am. J. Epidemiol. 160 (2004), 977–984.
7. Ascherio, A., Chen, H., Schwarzschild, M., Zhang, S., Colditz, G., Speizer, F., Caffeine, postmenopausal estrogen, and risk of Parkinson's disease. Neurology 60 (2003), 790–795.
8. Baldereschi, M., Di Carlo, A., Rocca, W.A., Vanni, P., Maggi, S., Perissinotto, E., Grigoletto, F., Amaducci, L., Inzitari, D., Parkinson's disease and parkinsonism in a longitudinal study: two-fold higher incidence in men. ILSA Working Group. Italian Longitudinal Study on Aging. Neurology 55 (2000), 1358–1363.
9. Baraka, A.M., Korish, A.A., Soliman, G.A., Kamal, H., The possible role of estrogen and selective estrogen receptor modulators in a rat model of Parkinson's disease. Life Sci. 88 (2011), 879–885.
10. Bernheimer, H., Birkmayer, W., Hornykiewicz, O., Jellinger, K., Seitelberger, F., Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 20 (1973), 415–455.
11. Beyer, C., Pilgrim, C., Reisert, I., Dopamine content and metabolism in mesencephalic and diencephalic cell cultures: sex differences and effects of sex steroids. J. Neurosci. 11 (1991), 1325–1333.
12. Bode, F.J., Stephan, M., Suhling, H., Pabst, R., Straub, R.H., Raber, K.A., Bonin, M., Nguyen, H.P., Riess, O., Bauer, A., Sjoberg, C., Petersen, A., von Horsten, S., Sex differences in a transgenic rat model of Huntington's disease: decreased 17beta-estradiol levels correlate with reduced numbers of DARPP32 + neurons in males. Hum. Mol. Genet. 17 (2008), 2595–2609.
13. Bortolato, M., Frau, R., Godar, S.C., Mosher, L.J., Paba, S., Marrosu, F., Devoto, P., The implication of neuroactive steroids in Tourette syndrome pathogenesis: a role for 5alpha-reductase?. J. Neuroendocrinol, 2013, 10.1111/jne.12066.
14. Bourque, M., Liu, B., Dluzen, D.E., Di Paolo, T., Tamoxifen protects male mice nigrostriatal dopamine against methamphetamine-induced toxicity. Biochem Pharmacol 74 (2007), 1413–1423.
15. Bourque, M., Dluzen, D.E., Paolo, T.D., Neuroprotective actions of sex steroids in Parkinson's disease. Front. Neuroendocrinol. 30 (2009), 142–157.
16. Brown, T.P., Rumsby, P.C., Capleton, A.C., Rushton, L., Levy, L.S., Pesticides and Parkinson's disease—is there a link?. Environ. Health Perspect. 114 (2006), 156–164.
17. Callier, S., Morissette, M., Grandbois, M., Di Paolo, T., Stereospecific prevention by 17beta-estradiol of MPTP-induced dopamine depletion in mice. Synapse 37 (2000), 245–251.
18. Callier, S., Morissette, M., Grandbois, M., Pelaprat, D., Di Paolo, T., Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice. Synapse 41 (2001), 131–138.
19. Campos, F.L., Cristovao, A.C., Rocha, S.M., Fonseca, C.P., Baltazar, G., GDNF contributes to oestrogen-mediated protection of midbrain dopaminergic neurones. J. Neuroendocrinol. 24 (2012), 1386–1397.
20. Cantuti-Castelvetri, Effects of gender on nigral gene expression and Parkinson disease. Neurobiol. Dis., 2007, 1–9.
21. Carruth, L., Reisert, I., Arnold, A., Sex chromosome genes directly affect brain sexual differentiation. Nat. Neurosci. 5 (2002), 933–934.
22. Cereda, E., Barichella, M., Cassani, E., Caccialanza, R., Pezzoli, G., Reproductive factors and clinical features of Parkinson's disease. Parkinsonism Relat. Disord., 2013, 1–6.
23. Chen, X., Grisham, W., Arnold, A., X chromosome number causes sex differences in gene expression in adult mouse striatum. Eur. J. Neurosci. 29 (2009), 768–776.
24. Cordellini, M.F., Piazzetta, G., Pinto, K.C., Delattre, A.M., Matheussi, F., Carolino, R.O., Szawka, R.E., Anselmo-Franci, J.A., Ferraz, A.C., Effect of different doses of estrogen on the nigrostriatal dopaminergic system in two 6-hydroxydopamine-induced lesion models of Parkinson's disease. Neurochem Res 36 (2011), 955–961.
25. Currie, L.J., Harrison, M.B., Trugman, J.M., Bennett, J.P., Wooten, G.F., Postmenopausal estrogen use affects risk for Parkinson disease. Arch. Neurol. 61 (2004), 886–888.
26. Czech, D., Lee, J., Sim, H., Parish, C., Vilain, E., Harley, V., The human testis-determining factor SRY localizes in midbrain dopamine neurons and regulates multiple components of catecholamine synthesis and metabolism. J. Neurochem. 122 (2012), 260–271.
27. D'Astous, M., Morissette, M., Tanguay, B., Callier, S., Di Paolo, T., Dehydroepiandrosterone (DHEA) such as 17beta-estradiol prevents MPTP-induced dopamine depletion in mice. Synapse 47 (2003), 10–14.
28. D'Astous, M., Morissette, M., Di Paolo, T., Effect of estrogen receptor agonists treatment in MPTP mice: evidence of neuroprotection by an ER alpha agonist. Neuropharmacology 47 (2004), 1180–1188.
29. D'Astous, M., Gajjar, T.M., Dluzen, D.E., Di Paolo, T., Dopamine transporter as a marker of neuroprotection in methamphetamine-lesioned mice treated acutely with estradiol. Neuroendocrinology 79 (2004), 296–304.
30. D'Astous, M., Mickley, K.R., Dluzen, D.E., Di Paolo, T., Differential protective properties of estradiol and tamoxifen against methamphetamine-induced nigrostriatal dopaminergic toxicity in mice. Neuroendocrinology 82 (2005), 111–120.
31. D'Astous, M., Morissette, M., Callier, S., Di Paolo, T., Regulation of striatal preproenkephalin mRNA levels in MPTP-lesioned mice treated with estradiol. J Neurosci Res 80 (2005), 138–144.
32. DeGiorgio, L.A., Attardi, B., Shimizu, Y., Ogata, M., Volpe, B.T., 17 beta-estradiol treatment retards excitotoxic delayed degeneration in substantia nigra reticulata neurons. Brain Res 936 (2002), 15–20.
33. Dewing, P., Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol. Brain Res., 2003, 1–9.
34. Dewing, P., Direct regulation of adult brain function by the male-specific factor SRY. Curr. Biol., 2006, 1–6.
35. 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.
36. 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.
37. Dluzen, D., Estrogen decreases corpus striatal neurotoxicity in response to 6-hydroxydopamine. Brain Res 767 (1997), 340–344.
38. 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.
39. Dluzen, D.E., Anderson, L.I., Pilati, C.F., Methamphetamine-gonadal steroid hormonal interactions: effects upon acute toxicity and striatal dopamine concentrations. Neurotoxicol. Teratol. 24 (2002), 267–273.
40. Dorner, J.L., Miller, B.R., Barton, S.J., Brock, T.J., Rebec, G.V., Sex differences in behavior and striatal ascorbate release in the 140 CAG knock-in mouse model of Huntington's disease. Behav. Brain Res. 178 (2007), 90–97.
41. Ekue, A., Boulanger, J.F., Morissette, M., Di Paolo, T., Lack of effect of testosterone and dihydrotestosterone compared to 17beta-oestradiol in 1-methyl-4-phenyl-1,2,3,6, tetrahydropyridine-mice. J. Neuroendocrinol. 14 (2002), 731–736.
42. Fahn, S., Jankovic, J., Hallett, M., Principles and Practice of Movement Disorders. 2011.
43. Ferraz, A.C., Xavier, L.L., Hernandes, S., Sulzbach, M., Viola, G.G., Anselmo-Franci, J.A., Achaval, M., Da Cunha, C., 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.
44. Ferraz, A.C., Matheussi, F., Szawka, R.E., Rizelio, V., Delattre, A.M., Rigon, P., Hermel Edo, E., Xavier, L.L., Achaval, M., Anselmo-Franci, J.A., Evaluation of estrogen neuroprotective effect on nigrostriatal dopaminergic neurons following 6-hydroxydopamine injection into the substantia nigra pars compacta or the medial forebrain bundle. Neurochem. Res. 33 (2008), 1238–1246.
45. Foroud, T., Gray, J., Ivashina, J., Conneally, P.M., Differences in duration of Huntington's disease based on age at onset. J. Neurol. Neurosurg. Psychiatry 66 (1999), 52–56.
46. Gao, X., Dluzen, D.E., Tamoxifen abolishes estrogen's neuroprotective effect upon methamphetamine neurotoxicity of the nigrostriatal dopaminergic system. Neuroscience 103:2 (2001), 385–394.
47. Gao, X., Dluzen, D.E., The effect of testosterone upon methamphetamine neurotoxicity of the nigrostriatal dopaminergic system. Brain Res. 892 (2001), 63–69.
48. Gajjar, T.M., Anderson, L.I., Dluzen, D.E., Acute effects of estrogen upon methamphetamine induced neurotoxicity of the nigrostriatal dopaminergic system. J. Neural Transm. 110 (2003), 1215–1224.
49. Gardiner, S.A., Morrison, M.F., Mozley, P.D., Mozley, L.H., 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 12 (2004), 621–630.
50. Gillies, G.E., McArthur, S., Independent influences of sex steroids of systemic and central origin in a rat model of Parkinson's disease: a contribution to sex-specific neuroprotection by estrogens. Horm. Behav. 57 (2010), 23–34.
51. Goodenough, S., Schleusner, D., Pietrzik, C., Skutella, T., Behl, C., Glycogen synthase kinase 3beta links neuroprotection by 17beta-estradiol to key Alzheimer processes. Neuroscience 132 (2005), 581–589.
52. Goodman, Y., Bruce, A.J., Cheng, B., Mattson, M.P., Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J. Neurochem. 66 (1996), 1836–1844.
53. 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.
54. Heron, P., Daya, S., 17beta-Estradiol protects against quinolinic acid-induced lipid peroxidation in the rat brain. Metab. Brain Dis. 15 (2000), 267–274.
55. Hirohata, M., Ono, K., Morinaga, A., Ikeda, T., Yamada, M., Anti-aggregation and fibril-destabilizing effects of sex hormones on α-synuclein fibrils in vitro. Exp. Neurol. 217 (2009), 434–439.
56. Jankovic, J., Kurlan, R., Tourette syndrome: evolving concepts. Mov. Disord. 26 (2011), 1149–1156.
57. 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. 17 (2005), 509–517.
58. Koller, W.C., Barr, A., Biary, N., Estrogen treatment of dyskinetic disorders. Neurology 32 (1982), 547–549.
59. Kompoliti, K., Goetz, C.G., Leurgans, S., Raman, R., Comella, C.L., Estrogen, progesterone, and tic severity in women with Gilles de la Tourette syndrome. Neurology, 57, 2001, 1519.
60. Kuiper, G.G., Carlsson, B., Grandien, K., Enmark, E., Haggblad, J., Nilsson, S., Gustafsson, J.A., Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138 (1997), 863–870.
61. Kuppers, E., Beyer, C., Expression of estrogen receptor-alpha and beta mRNA in the developing and adult mouse striatum. Neurosci. Lett. 276 (1999), 95–98.
62. Laakso, A., Vilkman, H., Bergman, J., Haaparanta, M., Solin, O., Syvalahti, E., Salokangas, R.K., Hietala, J., Sex differences in striatal presynaptic dopamine synthesis capacity in healthy subjects. Biol. Psychiatry 52 (2002), 759–763.
63. Latourelle, J.C., Dybdahl, M., Destefano, A.L., Myers, R.H., Lash, T.L., Risk of Parkinson's disease after tamoxifen treatment. BMC Neurol., 10, 2010, 23.
64. Lavalaye, J., Booij, J., Reneman, L., Habraken, J.B., van Royen, E.A., Effect of age and gender on dopamine transporter imaging with [123I]FP-CIT SPET in healthy volunteers. Eur. J. Nucl. Med. 27 (2000), 867–869.
65. Le Saux, M., Di Paolo, T., Influence of oestrogenic compounds on monoamine transporters in rat striatum. J. Neuroendocrinol. 18 (2006), 25–32.
66. Leckman, J.F., Scahill, L., Possible exacerbation of tics by androgenic steroids. N. Engl. J. Med., 322, 1990, 1674.
67. Lewis, C., Dluzen, D.E., Testosterone enhances dopamine depletion by methamphetamine in male, but not female, mice. Neurosci Lett 448 (2008), 130–133.
68. Liu, B., Dluzen, D.E., Effect of estrogen upon methamphetamine-induced neurotoxicity within the impaired nigrostriatal dopaminergic system. Synapse 60 (2006), 354–361.
69. Liu, L.X., Chen, W.F., Xie, J.X., Wong, M.S., Neuroprotective effects of genistein on dopaminergic neurons in the mice model of Parkinson's disease. Neurosci. Res. 60 (2008), 156–161.
70. Marder, K., Tang, M., Alfaro, B., Mejia, H., Cote, L., Jacobs, D., Stern, Y., Sano, M., Mayeux, R., Postmenopausal estrogen use and Parkinson's disease with and without dementia. Neurology 50 (1998), 1141–1143.
71. Mickley, K.R., Dluzen, D.E., Dose-response effects of estrogen and tamoxifen upon methamphetamine-induced behavioral responses and neurotoxicity of the nigrostriatal dopaminergic system in female mice. Neuroendocrinology 79 (2004), 305–316.
72. McFarland, K., Price, D.L., Davis, C.N., Ma, J.N., Bonhaus, D.W., Burstein, E.S., Olsson, R., AC-186, a selective nonsteroidal estrogen receptor beta agonist, shows gender specific neuroprotection in a Parkinson's disease rat model. ACS Chem Neurosci 4 (2013), 1249–1255.
73. 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.
74. Morissette, M., Di Paolo, T., Effect of estradiol on striatal dopamine activity of female hemiparkinsonian monkeys. J. Neurosci. Res. 87 (2009), 1634–1644.
75. Morissette, M., Al Sweidi, S., Callier, S., Di Paolo, T., Estrogen and SERM neuroprotection in animal models of Parkinson's disease. Mol. Cell. Endocrinol. 290 (2008), 60–69.
76. Muroni, A., Paba, S., Puligheddu, M., Marrosu, F., Bortolato, M., A preliminary study of finasteride in Tourette syndrome. Mov. Disord. 26 (2011), 2146–2147.
77. Murray, H.E., Pillai, A.V., McArthur, S.R., Razvi, N., Datla, K.P., Dexter, D.T., 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.
78. Myers, R.E., Anderson, L.I., Dluzen, D.E., Estrogen, but not testosterone, attenuates methamphetamine-evoked dopamine output from superfused striatal tissue of female and male mice. Neuropharmacology 44 (2003), 624–632.
79. Ohtani, H., Nomoto, M., Douchi, T., Chronic estrogen treatment replaces striatal dopaminergic function in ovariectomized rats. Brain Res. 900 (2001), 163–168.
80. Okun, M.S., Fernandez, H.H., Rodriguez, R.L., Romrell, J., Suelter, M., Munson, S., Louis, E.D., Mulligan, T., Foster, P.S., Shenal, B.V., Armaghani, S.J., Jacobson, C., Wu, S., Crucian, G., Testosterone therapy in men with Parkinson disease: results of the TEST-PD Study. Arch. Neurol. 63 (2006), 729–735.
81. Olsson, R., AC-186 a selective nonsteroidal estrogen receptor agonist, shows gender specific neuroprotection in a Parkinson's disease rat model. ACS Chem. Neurosci., 2013, 1–7.
82. Ookubo, M., Yokoyama, H., Takagi, S., Kato, H., Araki, T., Effects of estrogens on striatal damage after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity in male and female mice. Mol. Cell. Endocrinol. 296 (2008), 87–93.
83. Palacios, N., Gao, X., Mccullough, M., Schwarzschild, M., Shah, R., Gapstur, S., Ascherio, A., Caffeine and risk of Parkinson's disease in a large cohort of men and women. Mov. Disord. 27 (2012), 1276–1282.
84. Pankratz, N., Nichols, W.C., Uniacke, S.K., Halter, C., Murrell, J., Rudolph, A., Shults, C.W., Conneally, P.M., Foroud, T., Genome-wide linkage analysis and evidence of gene-by-gene interactions in a sample of 362 multiplex Parkinson disease families. Hum. Mol. Genet. 12 (2003), 2599–2608.
85. Peterson, B.S., Leckman, J.F., Scahill, L., Naftolin, F., Keefe, D., Charest, N.J., Cohen, D.J., Steroid hormones and CNS sexual dimorphisms modulate symptom expression in Tourette's syndrome. Psychoneuroendocrinology 17 (1992), 553–563.
86. Pozzi, S., Benedusi, V., Maggi, A., Vegeto, E., Estrogen action in neuroprotection and brain inflammation. Ann. N. Y. Acad. Sci. 1089 (2006), 302–323.
87. Quinn, N.P., Marsden, C.D., Menstrual-related fluctuations in Parkinson's disease. Mov. Disord. 1 (1986), 85–87.
88. R S-P, D C, S N, B S, C B, Lipton, R., Role of endogenous and exogenous hormone exposure on the risk of Parkinson's disease. Annual Meeting of AAN. Seattle, Washington, 2009 (Abstract S23.002).
89. Raab, H., Pilgrim, C., Reisert, I., Effects of sex and estrogen on tyrosine hydroxylase mRNA in cultured embryonic rat mesencephalon. Brain Res. Mol. Brain Res. 33 (1995), 157–164.
90. Ragonese, P., D'Amelio, M., Salemi, G., Aridon, P., Gammino, M., Epifanio, A., Morgante, L., Savettieri, G., Risk of Parkinson disease in women: effect of reproductive characteristics. Neurology 62 (2004), 2010–2014.
91. Ramirez, A.D., Liu, X., Menniti, F.S., Repeated estradiol treatment prevents MPTP-induced dopamine depletion in male mice. Neuroendocrinology 77 (2003), 223–231.
92. Reisert, I., Pilgrim, C., Sexual differentiation of monoaminergic neurons—genetic or epigenetic?. Trends Neurosci. 14 (1991), 468–473.
93. Rocca, W., Bower, J., Maraganore, D., Ahlskog, J., Grossardt, B., De Andrade, M., Melton, L., Increased risk of parkinsonism in women who underwent oophorectomy before menopause. Neurology 70 (2008), 200–209.
94. Rodriguez-Navarro, J.A., Solano, R.M., Casarejos, M.J., Gomez, A., Perucho, J., de Yebenes, J.G., Mena, M.A., Gender differences and estrogen effects in parkin null mice. J. Neurochem. 106 (2008), 2143–2157.
95. Sawada, H., Ibi, M., Kihara, T., Urushitani, M., Akaike, A., Shimohama, S., Estradiol protects mesencephalic dopaminergic neurons from oxidative stress-induced neuronal death. J. Neurosci. Res. 54 (1998), 707–719.
96. Schwabe, M.J., Konkol, R.J., Menstrual cycle-related fluctuations of tics in Tourette syndrome. Pediatr. Neurol. 8 (1992), 43–46.
97. Session, D.R., Pearlstone, M.M., Jewelewicz, R., Kelly, A.C., Estrogens and Parkinson's disease. Med. Hypotheses 42 (1994), 280–282.
98. Shughrue, P.J., Estrogen attenuates the MPTP-induced loss of dopamine neurons from the mouse SNc despite a lack of estrogen receptors (ERalpha and ERbeta). Exp Neurol 190 (2004), 468–477.
99. Simon, K.C., Chen, H., Gao, X., Schwarzschild, M.A., Ascherio, A., Reproductive factors, exogenous estrogen use, and risk of Parkinson's disease. Mov. Disord. 24 (2009), 1359–1365.
100. Simpkins, J.W., Yi, K.D., Yang, S., Dykens, J.A., Mitochondrial mechanisms of estrogen neuroprotection. Biochim. Biophys. Acta Gen. Subj. 1800 (2010), 1113–1120.
101. Simunovic, F., Yi, M., Wang, Y., Stephens, R., Sonntag, K., Evidence for gender-specific transcriptional profiles of nigral dopamine neurons in Parkinson disease. PLoS ONE, 5, 2010, e8856.
102. Tao, Q., Fan, X., Li, T., Tang, Y., Yang, D., Le, W., Gender segregation in gene expression and vulnerability to oxidative stress induced injury in ventral mesencephalic cultures of dopamine neurons. J. Neurosci. Res. 90 (2011), 167–178.
103. Tripanichkul, W., Sripanichkulchai, K., Finkelstein, D.I., Estrogen down-regulates glial activation in male mice following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine intoxication. Brain Res 1084 (2006), 28–37.
104. Tsang, K., Ho, S., Lo, S., Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology 54 (2000), 2292–2298.
105. Tunez, I., Collado, J.A., Medina, F.J., Pena, J., Del, C.M.M., Jimena, I., Franco, F., Rueda, I., Feijoo, M., Muntane, J., Montilla, P., 17 beta-Estradiol may affect vulnerability of striatum in a 3-nitropropionic acid-induced experimental model of Huntington's disease in ovariectomized rats. Neurochem. Int. 48 (2006), 367–373.
106. van Dyck, C.H., Seibyl, J.P., Malison, R.T., Laruelle, M., Wallace, E., Zoghbi, S.S., Zea-Ponce, Y., Baldwin, R.M., Charney, D.S., Hoffer, P.B., Age-related decline in striatal dopamine transporter binding with iodine-123-beta-CITSPECT. J. Nucl. Med. 36 (1995), 1175–1181.
107. Wang, J., Green, P.S., Simpkins, J.W., Estradiol protects against ATP depletion, mitochondrial membrane potential decline and the generation of reactive oxygen species induced by 3-nitroproprionic acid in SK-N-SH human neuroblastoma cells. J. Neurochem. 77 (2001), 804–811.
108. Weaver, C.E.J., Park-Chung, M., Gibbs, T.T., Farb, D.H., 17beta-Estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors. Brain Res. 761 (1997), 338–341.
109. Wong, K.K., Müller, M.L., Kuwabara, H., Studenski, S.A., Bohnen, N., Gender differences in nigrostriatal dopaminergic innervation are present at young-to-middle but not at older age in normal adults. J. Clin. Neurosci. 19 (2012), 183–184.
110. Wooten, G.F., Currie, L.J., Bovbjerg, V.E., Lee, J.K., Patrie, J., Are men at greater risk for Parkinson's disease than women?. J. Neurol. Neurosurg. Psychiatry 75 (2004), 637–639.
111. Wu, J., Chen, K., Li, Y., Lau, Y., Shih, J., Regulation of monoamine oxidase A by the SRY gene on the Y chromosome. FASEB J. 23 (2009), 4029–4038.
112. Xu, K., Estrogen prevents neuroprotection by caffeine in the mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neurosci. 26 (2006), 535–541.
113. Yu, L., Liao, P.C., Estrogen and progesterone distinctively modulate methamphetamine-induced dopamine and serotonin depletions in C57BL/6J mice. J. Neural Transm. 107 (2000), 1139–1147.
114. Yu, L., Kuo, Y., Cherng, C.G., Chen, H.H., Hsu, C.H., Ovarian hormones do not attenuate methamphetamine-induced dopaminergic neurotoxicity in mice gonadectomized at 4 weeks postpartum. Neuroendocrinology 75 (2002), 282–287.
115. Zielonka, D., Marinus, J., Roos, R.A., Michele, G.D., Donato, S.D., Putter, H., Marcinkowski, J., Squitieri, F., Bentivoglio, A.R., Landwehrmeyer, G.B., The influence of gender on phenotype and disease progression in patients with Huntington's disease. Parkinsonism Relat. Disord. 19 (2013), 192–197.