Neuroactive gonadal drugs for neuroprotection in male and female models of Parkinson's disease

Neuroscience and Biobehavioral Reviews

Volumn 67, Issue , 2016, Pages 79-88

  Litim, Nadhir ^a,b   Morissette, Marc ^a   Di Paolo, Thérèse ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

6 OHDA; Dopamine; Dutasteride; Estrogen; Finasteride; G1; GPER1; MPTP; Neuroprotection; Parkinson's disease; PPT; Striatum

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 17ALPHA ESTRADIOL; AMANTADINE; ANDROSTANOLONE; ANTIPARKINSON AGENT; DIARYLPROPIONITRILE; DUTASTERIDE; ESTRADIOL; ESTRIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTRONE; FINASTERIDE; LEVODOPA; PRASTERONE; PROGESTERONE; RALOXIFENE; RASAGILINE; SELEGILINE; TAMOXIFEN; TESTOSTERONE; DOPAMINE; NEUROPROTECTIVE AGENT;

BIOLOGICAL MODEL; CELL SURVIVAL; DISEASE COURSE; DOPAMINERGIC NERVE CELL; DRUG EFFICACY; HUMAN; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; ANIMAL; DISEASE MODEL; FEMALE; MALE;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; ESTROGENS; FEMALE; HUMANS; MALE; NEUROPROTECTION; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE;

EID: 84951735123     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2015.09.024     Document Type: Review

References (140)

1. Adams, C., Kumar, R., The effect of estrogen in a man with Parkinson's disease and a review of its therapeutic potential. Int. J. Neurosci. 123 (2013), 741–742, 10.3109/00207454.2013.797903.
2. Almey, A., Filardo, E.J., Milner, T.A., Brake, W.G., Estrogen receptors are found in glia and at extranuclear neuronal sites in the dorsal striatum of female rats: evidence for cholinergic but not dopaminergic colocalization. Endocrinology 153 (2012), 5373–5383, 10.1210/en.2012-1458.
3. Alves, G., Müller, B., Herlofson, K., HogenEsch, I., Telstad, W., Aarsland, D., Tysnes, O.-B., Larsen, J.P., Norwegian ParkWest study group. Incidence of Parkinson's disease in Norway: the Norwegian ParkWest study. J. Neurol. Neurosurg. Psychiatry 80 (2009), 851–857, 10.1136/jnnp.2008.168211.
4. Anglade, P., Vyas, S., Javoy-Agid, F., Herrero, M.T., Michel, P.P., Marquez, J., Mouatt-Prigent, A., Ruberg, M., Hirsch, E.C., Agid, Y., Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12 (1997), 25–31.
5. Azcoitia, I., Arevalo, M.-A., De Nicola, A.F., Garcia-Segura, L.M., Neuroprotective actions of estradiol revisited. Trends Endocrinol. Metab. 22 (2011), 467–473, 10.1016/j.tem.2011.08.002.
6. Baba, Y., Putzke, J.D., Whaley, N.R., Wszolek, Z.K., Uitti, R.J., Gender and the Parkinson's disease phenotype. J. Neurol. 252 (2005), 1201–1205, 10.1007/s00415-005-0835-7.
7. 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.
8. 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, 10.1016/j.lfs.2011.03.010.
9. Bastide, M.F., Meissner, W.G., Picconi, B., Fasano, S., Fernagut, P.-O., Feyder, M., Francardo, V., Alcacer, C., Ding, Y., Brambilla, R., Fisone, G., Jon Stoessl, A., Bourdenx, M., Engeln, M., Navailles, S., De Deurwaerdère, P., Ko, W.K.D., Simola, N., Morelli, M., Groc, L., Rodriguez, M.-C., Gurevich, E.V., Quik, M., Morari, M., Mellone, M., Gardoni, F., Tronci, E., Guehl, D., Tison, F., Crossman, A.R., Kang, U.J., Steece-Collier, K., Fox, S., Carta, M., Angela Cenci, M., Bezard, E., Pathophysiology of L-dopa-induced motor and non-motor complications in Parkinson's disease. Prog. Neurobiol., 2015, 10.1016/j.pneurobio.2015.07.002.
10. Benedetti, M.D., Maraganore, D.M., Bower, J.H., McDonnell, S.K., Peterson, B.J., Ahlskog, J.E., Schaid, D.J., Rocca, W.A., Hysterectomy, menopause, and estrogen use preceding Parkinson's disease: an exploratory case–control study. Mov. Disord. 16 (2001), 830–837.
11. Blanchet, P.J., Fang, J., Hyland, K., Arnold, L.A., Mouradian, M.M., Chase, T.N., Short-term effects of high-dose 17beta-estradiol in postmenopausal PD patients: a crossover study. Neurology 53 (1999), 91–95.
12. Bologa, C.G., Revankar, C.M., Young, S.M., Edwards, B.S., Arterburn, J.B., Kiselyov, A.S., Parker, M.A., Tkachenko, S.E., Savchuck, N.P., Sklar, L.A., Oprea, T.I., Prossnitz, E.R., Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2 (2006), 207–212, 10.1038/nchembio775.
13. Bortolato, M., Cannas, A., Solla, P., Bini, V., Puligheddu, M., Marrosu, F., Finasteride attenuates pathological gambling in patients with Parkinson disease. J. Clin. Psychopharmacol. 32 (2012), 424–425, 10.1097/JCP.0b013e3182549c2a.
14. Bortolato, M., Devoto, P., Roncada, P., Frau, R., Flore, G., Saba, P., Pistritto, G., Soggiu, A., Pisanu, S., Zappala, A., Ristaldi, M.S., Tattoli, M., Cuomo, V., Marrosu, F., Barbaccia, M.L., Isolation rearing-induced reduction of brain 5α-reductase expression: relevance to dopaminergic impairments. Neuropharmacology 60 (2011), 1301–1308, 10.1016/j.neuropharm.2011.01.013.
15. Bortolato, M., Frau, R., Godar, S.C., Mosher, L.J., Paba, S., Marrosu, F., Devoto, P., The implication of neuroactive steroids in Tourette's syndrome pathogenesis: a role for 5α-reductase?. J. Neuroendocrinol. 25 (2013), 1196–1208, 10.1111/jne.12066.
16. Bortolato, M., Frau, R., Orrù, M., Bourov, Y., Marrosu, F., Mereu, G., Devoto, P., Gessa, G.L., Antipsychotic-like properties of 5-alpha-reductase inhibitors. Neuropsychopharmacology 33 (2008), 3146–3156, 10.1038/npp.2008.39.
17. Bourque, M., Dluzen, D.E., Di Paolo, T., Signaling pathways mediating the neuroprotective effects of sex steroids and SERMs in Parkinson's disease. Front. Neuroendocrinol. 33 (2012), 169–178, 10.1016/j.yfrne.2012.02.003.
18. Bourque, M., Dluzen, D.E., Di Paolo, T., Sex and temporally-dependent effects of methamphetamine toxicity on dopamine markers and signaling pathways. Neuropharmacology 62 (2012), 2363–2372, 10.1016/j.neuropharm.2012.02.009.
19. Bourque, M., Liu, B., Dluzen, D.E., Di Paolo, T., Sex differences in methamphetamine toxicity in mice: effect on brain dopamine signaling pathways. Psychoneuroendocrinology 36 (2011), 955–969, 10.1016/j.psyneuen.2010.12.007.
20. Bourque, M., Morissette, M., Côté, M., Soulet, D., Di Paolo, T., Implication of GPER1 in neuroprotection in a mouse model of Parkinson's disease. Neurobiol. Aging 34 (2013), 887–901, 10.1016/j.neurobiolaging.2012.05.022.
21. Bourque, M., Morissette, M., Di Paolo, T., Neuroprotection in Parkinsonian-treated mice via estrogen receptor α activation requires G protein-coupled estrogen receptor 1. Neuropharmacology 95 (2015), 343–352, 10.1016/j.neuropharm.2015.04.006.
22. Bourque, M., Morissette, M., Di Paolo, T., Raloxifene activates G protein-coupled estrogen receptor 1/Akt signaling to protect dopamine neurons in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice. Neurobiol. Aging 35 (2014), 2347–2356, 10.1016/j.neurobiolaging.2014.03.017.
23. Brailoiu, E., Dun, S.L., Brailoiu, G.C., Mizuo, K., Sklar, L.A., Oprea, T.I., Prossnitz, E.R., Dun, N.J., Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 193 (2007), 311–321, 10.1677/JOE-07-0017.
24. Brunsing, R.L., Prossnitz, E.R., Induction of interleukin-10 in the T helper type 17 effector population by the G protein coupled estrogen receptor (GPER) agonist G-1. Immunology 134 (2011), 93–106, 10.1111/j.1365-2567.2011.03471.x.
25. Bryant, D.N., Bosch, M.A., Rønnekleiv, O.K., Dorsa, D.M., 17-Beta estradiol rapidly enhances extracellular signal-regulated kinase 2 phosphorylation in the rat brain. Neuroscience 133 (2005), 343–352, 10.1016/j.neuroscience.2005.02.024.
26. 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, 10.1002/1098-2396(20000915)37:4<245::AID-SYN1>3.0.CO;2-5.
27. Callier, S., Morissette, M., Grandbois, M., Pélaprat, D., Di Paolo, T., Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice. Synapse 41 (2001), 131–138, 10.1002/syn.1067.
28. Cereda, E., Barichella, M., Cassani, E., Caccialanza, R., Pezzoli, G., Reproductive factors and clinical features of Parkinson's disease. Parkinsonism Relat. Disord. 19 (2013), 1094–1099, 10.1016/j.parkreldis.2013.07.020.
29. Chakrabarti, S., Davidge, S.T., G-protein coupled receptor 30 (GPR30): a novel regulator of endothelial inflammation. PLoS ONE, 7, 2012, e52357, 10.1371/journal.pone.0052357 (Epub 2012 December 20).
30. Chen, J., Hu, R., Ge, H., Duanmu, W., Li, Y., Xue, X., Hu, S., Feng, H., G-protein-coupled receptor 30-mediated antiapoptotic effect of estrogen on spinal motor neurons following injury and its underlying mechanisms. Mol. Med. Rep., 2015, 10.3892/mmr.2015.3601.
31. Cheng, H.C., Kim, S.R., Oo, T.F., Kareva, T., Yarygina, O., Rzhetskaya, M., Wang, C., During, M., Talloczy, Z., Tanaka, K., Komatsu, M., Kobayashi, K., Okano, H., Kholodilov, N., Burke, R.E., Akt suppresses retrograde degeneration of dopaminergic axons by inhibition of macroautophagy. J. Neurosci. 31 (2011), 2125–2135, 10.1523/JNEUROSCI.5519-10.2011.
32. Chu, C.T., Levinthal, D.J., Kulich, S.M., Chalovich, E.M., DeFranco, D.B., Oxidative neuronal injury. The dark side of ERK1/2. Eur. J. Biochem. 271 (2004), 2060–2066, 10.1111/j.1432-1033.2004.04132.x.
33. Connolly, B.S., Lang, A.E., Pharmacological treatment of Parkinson disease: a review. JAMA 311 (2014), 1670–1683, 10.1001/jama.2014.3654.
34. Côté, M., Bourque, M., Poirier, A.-A., Aubé, B., Morissette, M., Di Paolo, T., Soulet, D., GPER1-mediated immunomodulation and neuroprotection in the myenteric plexus of a mouse model of Parkinson's disease. Neurobiol. Dis. 82 (2015), 99–113, 10.1016/j.nbd.2015.05.017.
35. Cummings, J.A., Jagannathan, L., Jackson, L.R., Becker, J.B., Sex differences in the effects of estradiol in the nucleus accumbens and striatum on the response to cocaine: neurochemistry and behavior. Drug Alcohol Depend. 135 (2014), 22–28, 10.1016/j.drugalcdep.2013.09.009.
36. 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, 10.1001/archneur.61.6.886.
37. D'Astous, M., Mendez, P., Morissette, M., Garcia-Segura, L.M., Di Paolo, T., Implication of the phosphatidylinositol-3 kinase/protein kinase B signaling pathway in the neuroprotective effect of estradiol in the striatum of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice. Mol. Pharmacol. 69 (2006), 1492–1498, 10.1124/mol.105.018671.
38. 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, 10.1016/j.neuropharm.2004.08.020.
39. 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, 10.1002/syn.10145.
40. Daniel, J.M., Estrogens, estrogen receptors, and female cognitive aging: the impact of timing. Horm. Behav. 63 (2013), 231–237, 10.1016/j.yhbeh.2012.05.003.
41. Delmas, P.D., Bjarnason, N.H., Mitlak, B.H., Ravoux, A.C., Shah, A.S., Huster, W.J., Draper, M., Christiansen, C., Effects of raloxifene on bone mineral density, serum cholesterol concentrations, and uterine endometrium in postmenopausal women. N. Engl. J. Med. 337 (1997), 1641–1647, 10.1056/NEJM199712043372301.
42. Devoto, P., Frau, R., Bini, V., Pillolla, G., Saba, P., Flore, G., Corona, M., Marrosu, F., Bortolato, M., Inhibition of 5α-reductase in the nucleus accumbens counters sensorimotor gating deficits induced by dopaminergic activation. Psychoneuroendocrinology 37 (2012), 1630–1645, 10.1016/j.psyneuen.2011.09.018.
43. di Michele, F., Longone, P., Romeo, E., Lucchetti, S., Brusa, L., Pierantozzi, M., Bassi, A., Bernardi, G., Stanzione, P., Decreased plasma and cerebrospinal fluid content of neuroactive steroids in Parkinson's disease. Neurol. Sci. 24 (2003), 172–173, 10.1007/s10072-003-0115-1.
44. Dluzen, D.E., McDermott, J.L., Anderson, L.I., Tamoxifen eliminates estrogen's neuroprotective effect upon MPTP-induced neurotoxicity of the nigrostriatal dopaminergic system. Neurotox. Res. 3 (2001), 291–300.
45. 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.
46. Duka, T., Duka, V., Joyce, J.N., Sidhu, A., Alpha-Synuclein contributes to GSK-3beta-catalyzed Tau phosphorylation in Parkinson's disease models. FASEB J. 23 (2009), 2820–2830, 10.1096/fj.08-120410.
47. 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.
48. Elstner, M., Morris, C.M., Heim, K., Bender, A., Mehta, D., Jaros, E., Klopstock, T., Meitinger, T., Turnbull, D.M., Prokisch, H., Expression analysis of dopaminergic neurons in Parkinson's disease and aging links transcriptional dysregulation of energy metabolism to cell death. Acta Neuropathol. 122 (2011), 75–86, 10.1007/s00401-011-0828-9.
49. Fahn, S., The spectrum of levodopa-induced dyskinesias. Ann. Neurol., 47, 2000 S2-9-discussion-S9-11.
50. Fahn and the Parkinson Study Group, Does levodopa slow or hasten the rate of progression of Parkinson's disease?. J. Neurol., 252, 2005, 10.1007/s00415-005-4008-5 iv37–iv42.
51. Finn, D.A., Beadles-Bohling, A.S., Beckley, E.H., Ford, M.M., Gililland, K.R., Gorin-Meyer, R.E., Wiren, K.M., A new look at the 5alpha-reductase inhibitor finasteride. CNS Drug Rev. 12 (2006), 53–76, 10.1111/j.1527-3458.2006.00053.x.
52. Francardo, V., Bez, F., Wieloch, T., Nissbrandt, H., Ruscher, K., Cenci, M.A., Pharmacological stimulation of sigma-1 receptors has neurorestorative effects in experimental parkinsonism. Brain 137 (2014), 1998–2014, 10.1093/brain/awu107.
53. Frau, R., Bini, V., Pes, R., Pillolla, G., Saba, P., Devoto, P., Bortolato, M., Inhibition of 17α-hydroxylase/C17,20 lyase reduces gating deficits consequent to dopaminergic activation. Psychoneuroendocrinology 39 (2014), 204–213, 10.1016/j.psyneuen.2013.09.014.
54. Frau, R., Pillolla, G., Bini, V., Tambaro, S., Devoto, P., Bortolato, M., Inhibition of 5α-reductase attenuates behavioral effects of D1-, but not D2-like receptor agonists in C57BL/6 mice. Psychoneuroendocrinology 38 (2013), 542–551, 10.1016/j.psyneuen.2012.07.014.
55. Gao, H.-M., Hong, J.-S., Gene–environment interactions: key to unraveling the mystery of Parkinson's disease. Prog. Neurobiol. 94 (2011), 1–19, 10.1016/j.pneurobio.2011.03.005.
56. Gingerich, S., Kim, G.L., Chalmers, J.A., Koletar, M.M., Wang, X., Wang, Y., Belsham, D.D., Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 170 (2010), 54–66, 10.1016/j.neuroscience.2010.06.076.
57. Golbe, L.I., Young-onset Parkinson's disease: a clinical review. Neurology 41 (1991), 168–173.
58. 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.
59. Haaxma, C.A., Bloem, B.R., Borm, G.F., Oyen, W.J.G., Leenders, K.L., Eshuis, S., Booij, J., Dluzen, D.E., Horstink, M.W.I.M., Gender differences in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 78 (2007), 819–824, 10.1136/jnnp.2006.103788.
60. Hammes, S.R., Levin, E.R., Extranuclear steroid receptors: nature and actions. Endocr. Rev. 28 (2007), 726–741, 10.1210/er.2007-0022.
61. Hauser, R.A., Rascol, O., Korczyn, A.D., Jon Stoessl, A., Watts, R.L., Poewe, W., De Deyn, P.P., Lang, A.E., Ten-year follow-up of Parkinson's disease patients randomized to initial therapy with ropinirole or levodopa. Mov. Disord. 22 (2007), 2409–2417.
62. Hayashi, T., Su, T.-P., Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 18 (2004), 269–284, 10.2165/00023210-200418050-00001.
63. Hetman, M., Gozdz, A., Role of extracellular signal regulated kinases 1 and 2 in neuronal survival. Eur. J. Biochem. 271 (2004), 2050–2055.
64. Hickey, P., Stacy, M., Available and emerging treatments for Parkinson's disease: a review. Drug Des. Dev. Ther. 5 (2011), 241–254, 10.2147/DDDT.S11836.
65. Hu, R., Sun, H., Zhang, Q., Chen, J., Wu, N., Meng, H., Cui, G., Hu, S., Li, F., Lin, J., Wan, Q., Feng, H., G-protein coupled estrogen receptor 1 mediated estrogenic neuroprotection against spinal cord injury. Crit. Care Med. 40 (2012), 3230–3237, 10.1097/CCM.0b013e3182657560.
66. Investigators, P.S.G.C.C., Long-term effect of initiating pramipexole vs. levodopa in early Parkinson disease. Arch. Neurol. 66 (2009), 563–570, 10.1001/archneur.66.1.nct90001.
67. Jackson-Lewis, V., Blesa, J., Przedborski, S., Animal models of Parkinson's disease. Parkinsonism Relat. Disord., 2012.
68. Jenner, P., Preclinical evidence for neuroprotection with monoamine oxidase-B inhibitors in Parkinson's disease. Neurology 63 (2004), S13–S22.
69. Jordan, V.C., SERMs: meeting the promise of multifunctional medicines. J. Natl. Cancer Inst. 99 (2007), 350–356, 10.1093/jnci/djk062.
70. Jordan, V.C., O'Malley, B.W., Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J. Clin. Oncol. 25 (2007), 5815–5824, 10.1200/JCO.2007.11.3886.
71. 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, 10.1111/j.1365-2826.2005.01337.x.
72. Kanda, N., Watanabe, S., 17beta-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J. Invest. Dermatol. 121 (2003), 1500–1509, 10.1111/j.1523-1747.2003.12617.x.
73. Kanda, N., Watanabe, S., Abstract of article: 17[beta]-Estradiol enhances the production of nerve growth factor in THP-1-derived macrophages or peripheral blood monocyte-derived macrophages. J. Invest. Dermatol., 2003.
74. Kuroki, Y., Fukushima, K., Kanda, Y., Mizuno, K., Watanabe, Y., Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur. J. Pharmacol. 400 (2000), 205–209.
75. Lang, A.E., The progression of Parkinson disease: a hypothesis. Neurology 68 (2007), 948–952, 10.1212/01.wnl.0000257110.91041.5d.
76. 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.
77. Lebesgue, D., Chevaleyre, V., Zukin, R.S., Etgen, A.M., Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection. Steroids, 2009.
78. Lebesgue, D., Traub, M., De Butte-Smith, M., Chen, C., Zukin, R.S., Kelly, M.J., Etgen, A.M., Acute administration of non-classical estrogen receptor agonists attenuates ischemia-induced hippocampal neuron loss in middle-aged female rats. PLoS ONE, 5, 2010, e8642, 10.1371/journal.pone.0008642.
79. Litim, N., Bourque, M., Al Sweidi, S., Morissette, M., Di Paolo, T., The 5α-reductase inhibitor Dutasteride but not Finasteride protects dopamine neurons in the MPTP mouse model of Parkinson's disease. Neuropharmacology 97 (2015), 86–94, 10.1016/j.neuropharm.2015.05.015.
80. Liu, R., Baird, D., Park, Y., Freedman, N.D., Huang, X., Hollenbeck, A., Blair, A., Chen, H., Female reproductive factors, menopausal hormone use, and Parkinson's disease. Mov. Disord. 29 (2014), 889–896, 10.1002/mds.25771.
81. Liu, S.-B., Han, J., Zhang, N., Tian, Z., Li, X.-B., Zhao, M.-G., Neuroprotective effects of oestrogen against oxidative toxicity through activation of G-protein-coupled receptor 30 receptor. Clin. Exp. Pharmacol. Physiol. 38 (2011), 577–585, 10.1111/j.1440-1681.2011.05549.x.
82. Liu, S.-B., Zhang, N., Guo, Y.-Y., Zhao, R., Shi, T.-Y., Feng, S.-F., Wang, S.-Q., Yang, Q., Li, X.-Q., Wu, Y.-M., Ma, L., Hou, Y., Xiong, L.-Z., Zhang, W., Zhao, M.-G., G-protein-coupled receptor 30 mediates rapid neuroprotective effects of estrogen via depression of NR2B-containing NMDA receptors. J. Neurosci. 32 (2012), 4887–4900, 10.1523/JNEUROSCI.5828-11.2012.
83. Lubomski, M., Louise Rushworth, R., Lee, W., Bertram, K.L., Williams, D.R., Sex differences in Parkinson's disease. J. Clin. Neurosci. 21 (2014), 1503–1506, 10.1016/j.jocn.2013.12.016.
84. Lundin, J.I., Ton, T.G.N., LaCroix, A.Z., Longstreth, W.T., Franklin, G.M., Swanson, P.D., Smith-Weller, T., Racette, B.A., Checkoway, H., Formulations of hormone therapy and risk of Parkinson's disease. Mov. Disord. 29 (2014), 1631–1636, 10.1002/mds.26037.
85. Lyons, K.E., Hubble, J.P., Tröster, A.I., Pahwa, R., Koller, W.C., Gender differences in Parkinson's disease. Clin. Neuropharmacol. 21 (1998), 118–121.
86. Maggiolini, M., Vivacqua, A., Fasanella, G., Recchia, A.G., Sisci, D., Pezzi, V., Montanaro, D., Musti, A.M., Picard, D., Andò, S., The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J. Biol. Chem. 279 (2004), 27008–27016, 10.1074/jbc.M403588200.
87. Malagelada, C., Jin, Z.H., Greene, L.A., RTP801 is induced in Parkinson's disease and mediates neuron death by inhibiting Akt phosphorylation/activation. J. Neurosci. 28 (2008), 14363–14371, 10.1523/JNEUROSCI.3928-08.2008.
88. Marder, K., Tang, M.X., 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.
89. Miller, D.B.D., Ali, S.F.S., O'Callaghan, J.P.J., Laws, S.C.S., The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann. N. Y. Acad. Sci. 844 (1998), 153–165, 10.1111/j.1749-6632.1998.tb08230.x.
90. Morrish, P.K., How valid is dopamine transporter imaging as a surrogate marker in research trials in Parkinson's disease?. Mov. Disord. 18:Suppl. 7 (2003), S63–S70, 10.1002/mds.10581.
91. Nitkowska, M., Czyżyk, M., Friedman, A., Reproductive life characteristics in females affected with Parkinson's disease and in healthy control subjects – a comparative study on Polish population. Neurol. Neurochir. Pol. 48 (2014), 322–327, 10.1016/j.pjnns.2014.08.004.
92. Nixon, E., Simpkins, J.W., Neuroprotective effects of nonfeminizing estrogens in retinal photoreceptor neurons. Invest. Ophthalmol. Vis. Sci. 53 (2012), 4739–4747, 10.1167/iovs.12-9517.
93. Okuda, C., Segal, D.S., Kuczenski, R., Deprenyl alters behavior and caudate dopamine through an amphetamine-like action. Pharmacol. Biochem. Behav. 43 (1992), 1075–1080, 10.1016/0091-3057(92)90484-W.
94. Olanow, C.W., Calne, D., Does selegiline monotherapy in Parkinson's disease act by symptomatic or protective mechanisms?. Neurology, 42, 1992 13-26-discussion-41-8.
95. Olanow, C.W., Hauser, R.A., Jankovic, J., A randomized, double-blind, placebo-controlled, delayed start study to assess rasagiline as a disease modifying therapy in Parkinson's disease (the ADAGIO study): rationale, design, and baseline characteristics. Mov. Disord. 23 (2008), 2194–2201, 10.1002/mds.22218.
96. Olanow, C.W., Obeso, J.A., Stocchi, F., Continuous dopamine-receptor treatment of Parkinson's disease: scientific rationale and clinical implications. Lancet Neurol. 5 (2006), 677–687, 10.1016/S1474-4422(06)70521-X.
97. Otto, C., Fuchs, I., Kauselmann, G., Kern, H., Zevnik, B., Andreasen, P., Schwarz, G., Altmann, H., Klewer, M., Schoor, M., Vonk, R., Fritzemeier, K.-H., GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol. Reprod. 80 (2009), 34–41, 10.1095/biolreprod.108.071175.
98. Paba, S., Frau, R., Godar, S.C., Devoto, P., Marrosu, F., Bortolato, M., Steroid 5α-reductase as a novel therapeutic target for schizophrenia and other neuropsychiatric disorders. Curr. Pharm. Des. 17 (2011), 151–167, 10.2174/138161211795049589.
99. Park, A., Stacy, M., Non-motor symptoms in Parkinson's disease. J. Neurol. 256 (2009), 293–298, 10.1007/s00415-009-5240-1.
100. Parkinson Study Group, A controlled trial of rasagiline in early Parkinson disease: the TEMPO Study. Arch. Neurol. 59 (2002), 1937–1943.
101. Parkinson Study Group, A randomized controlled trial comparing pramipexole with levodopa in early Parkinson's disease: design and methods of the CALM-PD Study. Parkinson Study Group. Clin. Neuropharmacol. 23 (2000), 34–44.
102. Parkinson Study Group, Effects of tocopherol and deprenyl on the progression of disability in early Parkinson's disease. N. Engl. J. Med. 328 (1993), 176–183, 10.1056/NEJM199301213280305.
103. Parkinson Study Group POETRY Investigators, A randomized pilot trial of estrogen replacement therapy in post-menopausal women with Parkinson's disease. Parkinsonism Relat. Disord. 17 (2011), 757–760, 10.1016/j.parkreldis.2011.07.007.
104. Petrone, A.B., Simpkins, J.W., Barr, T.L., 17β-estradiol and inflammation: implications for ischemic stroke. Aging Dis. 5 (2014), 340–345, 10.14336/AD.2014.0500340.
105. Petrovska, S., Dejanova, B., Jurisic, V., Estrogens: mechanisms of neuroprotective effects. J. Physiol. Biochem. 68 (2012), 455–460, 10.1007/s13105-012-0159-x.
106. Popat, R.A., Van Den Eeden, S.K., Tanner, C.M., McGuire, V., Bernstein, A.L., Bloch, D.A., Leimpeter, A., Nelson, L.M., Effect of reproductive factors and postmenopausal hormone use on the risk of Parkinson disease. Neurology 65 (2005), 383–390, 10.1212/01.wnl.0000171344.87802.94.
107. Pringsheim, T., Jette, N., Frolkis, A., Steeves, T.D.L., The prevalence of Parkinson's disease: a systematic review and meta-analysis. Mov. Disord. 29 (2014), 1583–1590, 10.1002/mds.25945.
108. Quesada, A., Lee, B.Y., Micevych, P.E., PI3 kinase/Akt activation mediates estrogen and IGF-1 nigral DA neuronal neuroprotection against a unilateral rat model of Parkinson's disease. Dev. Neurobiol. 68 (2008), 632–644, 10.1002/dneu.20609.
109. Quesada, A., Micevych, P.E., Estrogen interacts with the IGF-1 system to protect nigrostriatal dopamine and maintain motoric behavior after 6-hydroxdopamine lesions. J. Neurosci. Res. 75 (2004), 107–116, 10.1002/jnr.10833.
110. Quinn, N.P., Marsden, C.D., Menstrual-related fluctuations in Parkinson's disease. Mov. Disord. 1 (1986), 85–87, 10.1002/mds.870010112.
111. 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, 10.1212/WNL.62.11.2010.
112. Raz, L., Khan, M.M., Mahesh, V.B., Vadlamudi, R.K., Brann, D.W., Rapid estrogen signaling in the brain. Neurosignals 16 (2008), 140–153, 10.1159/000111559.
113. Revankar, C.M., Cimino, D.F., Sklar, L.A., Arterburn, J.B., Prossnitz, E.R., A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307 (2005), 1625–1630, 10.1126/science.1106943.
114. Rocca, W.A., Bower, J.H., Maraganore, D.M., Ahlskog, J.E., Grossardt, B.R., de Andrade, M., Melton, L.J., Increased risk of parkinsonism in women who underwent oophorectomy before menopause. Neurology 70 (2008), 200–209, 10.1212/01.wnl.0000280573.30975.6a.
115. Saunders-Pullman, R., Gordon-Elliott, J., Parides, M., Fahn, S., Saunders, H.R., Bressman, S., The effect of estrogen replacement on early Parkinson's disease. Neurology 52 (1999), 1417–1421, 10.1212/WNL.52.7.1417.
116. Schapira, A.H.V., Albrecht, S., Barone, P., Comella, C.L., McDermott, M.P., Mizuno, Y., Poewe, W., Rascol, O., Marek, K., Rationale for delayed-start study of pramipexole in Parkinson's disease: the PROUD study. Mov. Disord. 25 (2010), 1627–1632, 10.1002/mds.23143.
117. Schrag, A., Dyskinesias and motor fluctuations in Parkinson's disease: a community-based study. Brain 123 (2000), 2297–2305, 10.1093/brain/123.11.2297.
118. Shulman, L.M., Bhat, V., Gender disparities in Parkinson's disease. Expert Rev. Neurother. 6 (2006), 407–416, 10.1586/14737175.6.3.407.
119. 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, 10.1002/mds.22619.
120. Singh, M., Mechanisms of progesterone-induced neuroprotection. Ann. N. Y. Acad. Sci. 1052 (2005), 145–151, 10.1196/annals.1347.010.
121. Singh, M., Sétáló, G., Guan, X., Warren, M., Toran-Allerand, C.D., Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19 (1999), 1179–1188.
122. Soskić, V., Klemm, M., Proikas-Cezanne, T., Schwall, G.P., Poznanović, S., Stegmann, W., Groebe, K., Zengerling, H., Schoepf, R., Burnet, M., Schrattenholz, A., A connection between the mitochondrial permeability transition pore, autophagy, and cerebral amyloidogenesis. J. Proteome Res. 7 (2008), 2262–2269, 10.1021/pr700686x.
123. Stacy, M., Medical treatment of Parkinson disease. Neurol. Clin. 27 (2009), 605–631, 10.1016/j.ncl.2009.04.009.
124. Stacy, M., Galbreath, A., Optimizing long-term therapy for Parkinson disease: levodopa, dopamine agonists, and treatment-associated dyskinesia. Clin. Neuropharmacol. 31 (2008), 51–56, 10.1097/WNF.0b013e318065b088.
125. Stocchi, F., Optimising levodopa therapy for the management of Parkinson's disease. J. Neurol., 252(Suppl. 4), 2005, 10.1007/s00415-005-4009-4 IV43–IV48.
126. Su, T.P., London, E.D., Jaffe, J.H., Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems. Science 240 (1988), 219–221, 10.1126/science.2832949.
127. Sujith, O.K., Lane, C., Therapeutic options for continuous dopaminergic stimulation in Parkinson's disease. Ther. Adv. Neurol. Disord. 2 (2009), 105–113, 10.1177/1756285608101378.
128. Swerdlow, R.H., Parker, W.D., Currie, L.J., Bennett, J.P., Gender ratio differences between Parkinson's disease patients and their affected relatives. Parkinsonism Relat. Disord. 7 (2001), 129–133.
129. Tang, H., Zhang, Q., Yang, L., Dong, Y., Khan, M., Yang, F., Brann, D.W., Wang, R., GPR30 mediates estrogen rapid signaling and neuroprotection. Mol. Cell. Endocrinol. 387 (2014), 52–58, 10.1016/j.mce.2014.01.024.
130. Taylor, K.S.M., Cook, J.A., Counsell, C.E., Heterogeneity in male to female risk for Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 78 (2007), 905–906, 10.1136/jnnp.2006.104695.
131. Thomas, P., Pang, Y., Filardo, E.J., Dong, J., Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146 (2005), 624–632, 10.1210/en.2004-1064.
132. Tsang, K.L., Ho, S.L., Lo, S.K., Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology 54 (2000), 2292–2298.
133. Van Den Eeden, S.K., Tanner, C.M., Bernstein, A.L., Fross, R.D., Leimpeter, A., Bloch, D.A., Nelson, L.M., Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am. J. Epidemiol. 157 (2003), 1015–1022.
134. Vivacqua, A., Lappano, R., De Marco, P., Sisci, D., Aquila, S., De Amicis, F., Fuqua, S.A.W., Andò, S., Maggiolini, M., G protein-coupled receptor 30 expression is up-regulated by EGF and TGF alpha in estrogen receptor alpha-positive cancer cells. Mol. Endocrinol. 23 (2009), 1815–1826, 10.1210/me.2009-0120.
135. Whone, A.L., Watts, R.L., Stoessl, A.J., Davis, M., Reske, S., Nahmias, C., Lang, A.E., Rascol, O., Ribeiro, M.J., Remy, P., Poewe, W.H., Hauser, R.A., Brooks, D.J., REAL-PET Study Group, Slower progression of Parkinson's disease with ropinirole versus levodopa: the REAL-PET study. Ann. Neurol. 54 (2003), 93–101, 10.1002/ana.10609.
136. Wilson, M.E., Liu, Y., Wise, P.M., Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res. Mol. Brain Res. 102 (2002), 48–54.
137. Winklhofer, K.F., Haass, C., Mitochondrial dysfunction in Parkinson's disease. Biochim. Biophys. Acta 1802 (2010), 29–44, 10.1016/j.bbadis.2009.08.013.
138. 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.
139. Xu, Y., Dalrymple, S.L., Becker, R.E., Denmeade, S.R., Isaacs, J.T., Pharmacologic basis for the enhanced efficacy of dutasteride against prostatic cancers. Clin. Cancer Res. 12 (2006), 4072–4079, 10.1158/1078-0432.CCR-06-0184.
140. Youdim, M.B.H., Kupershmidt, L., Amit, T., Weinreb, O., Promises of novel multi-target neuroprotective and neurorestorative drugs for Parkinson's disease. Parkinsonism Relat. Disord. 20:Suppl. 1 (2014), S132–S136, 10.1016/S1353-8020(13)70032-4.