Effect of a chronic treatment with 17β-estradiol on striatal dopamine neurotransmission and the Akt/GSK3 signaling pathway in the brain of ovariectomized monkeys

Psychoneuroendocrinology

Volumn 37, Issue 2, 2012, Pages 280-291

  Sánchez, Maria Gabriela ^a,b   Morissette, Marc ^a,b   Di Paolo, Thérèse ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

17 Estradiol; Akt GSK3 signaling; Dopamine; Ovariectomized monkey

Indexed keywords

BETA TUBULIN; DOPAMINE TRANSPORTER; ESTRADIOL; GLYCOGEN SYNTHASE KINASE 3; PROTEIN KINASE B; SERINE; THREONINE; TYROSINE; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CAUDATE NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC TRANSMISSION; DRUG MECHANISM; ENZYME PHOSPHORYLATION; FEMALE; HAPLORHINI; LONG TERM CARE; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN BINDING; PUTAMEN; SIGNAL TRANSDUCTION;

ANIMALS; AUTORADIOGRAPHY; CAUDATE NUCLEUS; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ESTRADIOL; FEMALE; GLYCOGEN SYNTHASE KINASE 3; MACACA FASCICULARIS; OVARIECTOMY; PROTO-ONCOGENE PROTEINS C-AKT; PUTAMEN; SYNAPTIC TRANSMISSION; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 83555174360     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2011.06.012     Document Type: Article

References (55)

1. Adli M., Hollinde D.L., Stamm T., Wiethoff K., Tsahuridu M., Kirchheiner J., Heinz A., Bauer M. Response to lithium augmentation in depression is associated with the glycogen synthase kinase 3-beta -50T/C single nucleotide polymorphism. Biol. Psychiatry 2007, 62:1295-1302.
2. Akhondzadeh S., Nejatisafa A.A., Amini H., Mohammadi M.R., Larijani B., Kashani L., Raisi F., Kamalipour A. Adjunctive estrogen treatment in women with chronic schizophrenia: a double-blind, randomized, and placebo-controlled trial. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27:1007-1012.
3. Alimohamad H., Rajakumar N., Seah Y.H., Rushlow W. Antipsychotics alter the protein expression levels of beta-catenin and GSK-3 in the rat medial prefrontal cortex and striatum. Biol. Psychiatry 2005, 57:533-542.
4. Attali G., Weizman A., Gil-Ad I., Rehavi M. Opposite modulatory effects of ovarian hormones on rat brain dopamine and serotonin transporters. Brain Res. 1997, 756:153-159.
5. Beaulieu J.M., Gainetdinov R.R., Caron M.G. The Akt-GSK-3 signaling cascade in the actions of dopamine. Trends Pharmacol. Sci. 2007, 28:166-172.
6. Beaulieu J.M., Gainetdinov R.R., Caron M.G. Akt/GSK3 signaling in the action of psychotropic drugs. Annu. Rev. Pharmacol. Toxicol. 2009, 49:327-347.
7. Beaulieu J.M., Sotnikova T.D., Gainetdinov R.R., Caron M.G. Paradoxical striatal cellular signaling responses to psychostimulants in hyperactive mice. J. Biol. Chem. 2006, 281:32072-32080.
8. Beaulieu J.M., Sotnikova T.D., Yao W.D., Kockeritz L., Woodgett J.R., Gainetdinov R.R., Caron M.G. Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:5099-5104.
9. Benedetti F., Serretti A., Colombo C., Lorenzi C., Tubazio V., Smeraldi E. A glycogen synthase kinase 3-beta promoter gene single nucleotide polymorphism is associated with age at onset and response to total sleep deprivation in bipolar depression. Neurosci. Lett. 2004, 368:123-126.
10. Bosse R., Rivest R., Di Paolo T. Ovariectomy and estradiol treatment affect the dopamine transporter and its gene expression in the rat brain. Brain Res. Mol. Brain Res. 1997, 46:343-346.
11. Brami-Cherrier K., Valjent E., Garcia M., Pages C., Hipskind R.A., Caboche J. Dopamine induces a PI3-kinase-independent activation of Akt in striatal neurons: a new route to cAMP response element-binding protein phosphorylation. J. Neurosci. 2002, 22:8921.
12. Brooks D.J., Frey K.A., Marek K.L., Oakes D., Paty D., Prentice R., Shults C.W., Stoessl A.J. Assessment of neuroimaging techniques as biomarkers of the progression of Parkinson's disease. Exp. Neurol. 2003, 184(Suppl. 1):S68-S79.
13. Bryant D.N., Sheldahl L.C., Marriott L.K., Shapiro R.A., Dorsa D.M. Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine 2006, 29:199-207.
14. Cardona-Gomez G.P., Mendez P., Garcia-Segura L.M. Synergistic interaction of estradiol and insulin-like growth factor-I in the activation of PI3K/Akt signaling in the adult rat hypothalamus. Brain Res. Mol. Brain Res. 2002, 107:80-88.
15. Cardona-Gomez P., Perez M., Avila J., Garcia-Segura L.M., Wandosell F. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors GSK3, and beta-catenin in the hippocampus. Mol. Cell. Neurosci. 2004, 25:363-373.
16. Carvelli L., Moron J.A., Kahlig K.M., Ferrer J.V., Sen N., Lechleiter J.D., Leeb-Lundberg L.M., Merrill G., Lafer E.M., Ballou L.M., Shippenberg T.S., Javitch J.A., Lin R.Z., Galli A. PI 3-kinase regulation of dopamine uptake. J. Neurochem. 2002, 81:859-869.
17. Chalecka-Franaszek E., Chuang D.M. Lithium activates the serine/threonine kinase Akt 1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8745-8750.
18. Chen J.C., Chen P.C., Chiang Y.C. Molecular mechanisms of psychostimulant addiction. Chang Gung Med. J. 2009, 32:148-154.
19. Choi Y.C., Lee J.H., Hong K.W., Lee K.S. 17 Beta-estradiol prevents focal cerebral ischemic damages via activation of Akt and CREB in association with reduced PTEN phosphorylation in rats. Fundam. Clin. Pharmacol. 2004, 18:547-557.
20. 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. 2006, 69:1492-1498.
21. De Sarno P., Li X., Jope R.S. Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 2002, 43:1158-1164.
22. Dhandapani K.M., Brann D.W. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 2002, 67:1379-1385.
23. Di Paolo T. Modulation of brain dopamine transmission by sex steroids. Rev. Neurosci. 1994, 5:27-41.
24. Doolen S., Zahniser N.R. Protein tyrosine kinase inhibitors alter human dopamine transporter activity in Xenopus oocytes. J. Pharmacol. Exp. Ther. 2001, 296:931-938.
25. Emamian E.S., Hall D., Birnbaum M.J., Karayiorgou M., Gogos J.A. Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat. Genet. 2004, 36:131-137.
26. Garcia B.G., Wei Y., Moron J.A., Lin R.Z., Javitch J.A., Galli A. Akt is essential for insulin modulation of amphetamine-induced human dopamine transporter cell-surface redistribution. Mol. Pharmacol. 2005, 68:102-109.
27. 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 2004, 12:621-630.
28. Harwood A.J. Regulation of GSK-3: a cellular multiprocessor. Cell 2001, 105:821-824.
29. Honda K., Sawada H., Kihara T., Urushitani M., Nakamizo T., Akaike A., Shimohama S. Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J. Neurosci. Res. 2000, 60:321-327.
30. Hsiung S.C., Adlersberg M., Arango V., Mann J.J., Tamir H., Liu K.P. Attenuated 5 HT1A receptor signaling in brains of suicide victims: involvement of adenylyl cyclase, phosphatidylinositol 3-kinase, Akt and mitogen-activated protein kinase. J. Neurochem. 2003, 87:182-194.
31. 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.
32. Kalkman H.O. The role of the phosphatidylinositide 3-kinase-protein kinase B pathway in schizophrenia. Pharmacol. Ther. 2006, 110:117-134.
33. Karege F., Perroud N., Burkhardt S., Schwald M., Ballmann E., La Harpe R., Malafosse A. Alteration in kinase activity but not in protein levels of protein kinase B and glycogen synthase kinase-3beta in ventral prefrontal cortex of depressed suicide victims. Biol. Psychiatry 2007, 61:240-245.
34. Kulkarni J., de Castella A., Fitzgerald P.B., Gurvich C.T., Bailey M., Bartholomeusz C., Burger H. Estrogen in severe mental illness: a potential new treatment approach. Arch. Gen. Psychiatry 2008, 65:955-960.
35. Labrie F., Belanger A., Belanger P., Berube R., Martel C., Cusan L., Gomez J., Candas B., Chaussade V., Castiel I., Deloche C., Leclaire J. Metabolism of DHEA in postmenopausal women following percutaneous administration. J. Steroid Biochem. Mol. Biol. 2007, 103:178-188.
36. Le Saux M., Di Paolo T. Influence of oestrogenic compounds on monoamine transporters in rat striatum. J. Neuroendocrinol. 2006, 18:25-32.
37. 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. 2008, 28:14363-14371.
38. Martin R.F., Bowden D.M. Primate Brain Maps: Structure of the Macaque Brain 2000, Elsevier Science, Amsterdam, pp. 1-160.
39. Mendez P., Garcia-Segura L.M. Phosphatidylinositol 3-kinase and glycogen synthase kinase 3 regulate estrogen receptor-mediated transcription in neuronal cells. Endocrinology 2006, 147:3027-3039.
40. Morissette M., Di Paolo T. Effect of chronic estradiol and progesterone treatments of ovariectomized rats on brain dopamine uptake sites. J. Neurochem. 1993, 60:1876-1883.
41. Morissette M., Di Paolo T. Sex and estrous cycle variations of rat striatal dopamine uptake sites. Neuroendocrinology 1993, 58:16-22.
42. Morissette M., Di Paolo T. Effect of estradiol on striatal dopamine activity of female hemiparkinsonian monkeys. J. Neurosci. Res. 2009, 87:1634-1644.
43. Morissette M., Samadi P., Hadj Tahar A., Belanger N., Di Paolo T. Striatal Akt/GSK3 signaling pathway in the development of l-dopa-induced dyskinesias in MPTP monkeys. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:446-454.
44. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev. 1995, 20:91-127.
45. Rehavi M., Goldin M., Roz N., Weizman A. Regulation of rat brain vesicular monoamine transporter by chronic treatment with ovarian hormones. Brain Res. Mol. Brain Res. 1998, 57:31-37.
46. 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. 2008, 106:2143-2157.
47. Sánchez M.G., Bourque M., Morissette M., Di Paolo T. Steroids-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther. 2010, 16:e43-e71.
48. Scheid M.P., Woodgett J.R. PKB/AKT: functional insights from genetic models. Nat. Rev. Mol. Cell Biol. 2001, 2:760-768.
49. Serretti A., Benedetti F., Mandelli L., Calati R., Caneva B., Lorenzi C., Fontana V., Colombo C., Smeraldi E. Association between GSK-3beta -50T/C polymorphism and personality and psychotic symptoms in mood disorders. Psychiatry Res. 2008, 158:132-140.
50. 125I]RTI-121. Synapse 1995, 21:364-372.
51. Sulzer D., Sonders M.S., Poulsen N.W., Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 2005, 75:406-433.
52. Takahashi M., Tomizawa K., Kato R., Sato K., Uchida T., Fujita S.C., Imahori K. Localization and developmental changes of tau protein kinase I/glycogen synthase kinase 3 beta in rat brain. J. Neurochem. 1994, 63:245-255.
53. Wilson M.E., Liu Y., Wise P.M. Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res. Mol. Brain Res. 2002, 102:48-54.
54. Yang L.C., Zhang Q.G., Zhou C.F., Yang F., Zhang Y.D., Wang R.M., Brann D.W. Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One 2010, 5:e9851.
55. Zhao Z., Ksiezak-Reding H., Riggio S., Haroutunian V., Pasinetti G.M. Insulin receptor deficits in schizophrenia and in cellular and animal models of insulin receptor dysfunction. Schizophr. Res. 2006, 84:1-14.