Estrogen-mediated regulation of cholinergic expression in basal forebrain neurons requires extracellular-signal-regulated kinase activity

Neuroscience

Volumn 124, Issue 4, 2004, Pages 809-816

  Pongrac, J L ^a,b,c,d   Gibbs, R B ^b   Defranco, D B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

17 estradiol; Acetylcholine; ACh; Basal forebrain cholinergic neuron; BFCN; Bovine serum albumin; BSA; ChAT; Choline acetyltransferase; Choline transport; Days in vitro; DIV; E2; EDTA; ER; Estradiol; Ethylenediaminetetra acetic acid; NGF; Rat

Indexed keywords

ACETYLCHOLINE; CHOLINE; CHOLINE ACETYLTRANSFERASE; ESTROGEN; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; NERVE GROWTH FACTOR; SODIUM;

ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CHOLINE UPTAKE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME RELEASE; ESTROGEN ACTIVITY; ESTROGEN THERAPY; FEEDBACK SYSTEM; FOREBRAIN; HORMONE ACTION; NEUROENDOCRINE SYSTEM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RADIOMETRY; RAT; SECOND MESSENGER; TISSUE CULTURE;

ACETYLCHOLINE; ANIMALS; BINDING, COMPETITIVE; CELL SURVIVAL; CELLS, CULTURED; CHOLINE; CHOLINE O-ACETYLTRANSFERASE; ESTRADIOL; ESTROGENS; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; OXIDATIVE STRESS; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY;

EID: 1542321106     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.01.013     Document Type: Article

References (57)

1. Akova B., Surmen-Gur E., Gur H., Dirican M., Sarandol E., Kucukoglu S. Exercise-induced oxidative stress and muscle performance in healthy women Role of vitamin e supplementation and endogenous oestradiol. Eur J Appl Physiol. 84:2001;141-147.
2. Auld D.S., Mennicken F., Day J.C., Quirion R. Neurotrophins differentially enhance acetylcholine release, acetylcholine content and choline acetyltransferase activity in basal forebrain neurons. J Neurochem. 77:2001;253-262.
3. Bae Y.H., Hwang J.Y., Kim Y.H., Koh J.Y. Anti-oxidative neuroprotection by estrogens in mouse cortical cultures. J Korean Med Sci. 15:2000;327-336.
4. Bednarek-Tupikowska G., Bohdanowicz-Pawlak A., Bidzinska B., Milewicz A., Antonowicz-Juchniewicz J., Andrzejak R. Serum lipid peroxide levels and erythrocyte glutathione peroxidase and superoxide dismutase activity in premenopausal and postmenopausal women. Gynecol Endocrinol. 15:2001;298-303.
5. Behl C. Vitamin E protects neurons against oxidative cell death in vitro more effectively than 17-beta estradiol and induces the activity of the transcription factor NF-kappaB. J Neural Transm. 107:2000;393-407.
6. Beyer C., Raab H. Nongenomic effects of oestrogen Embryonic mouse midbrain neurons respond with a rapid release of calcium from intracellular stores. Eur J Neurosci. 10:1998;255-262.
7. Bhatnagar S.P., MacIntosh F.C. Effects of quaternary bases and inorganic cations on acetylcholine synthesis in nervous tissue. Can J Physiol Pharm. 45:1967;249-268.
8. Brinton R.D., Chen S., Montoya M., Hsieh D., Minaya J., Kim J., Chu H.-P. The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective. Neurobiol Aging. 21:2000;475-496.
9. Bottenstein J.E., Sato G.H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA. 76:1976;514-517.
10. Daniel J.M., Dohanich G.P. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci. 21:2001;6949-6956.
11. Fonnum F. Radiochemical microassays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J. 115:1969;465-479.
12. Gabor R., Nagle R., Johnson D.A., Gibbs R.B. Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res. 962:2003;244-247.
13. Gibbs R.B., Hashash A., Johnson D.A. Effects of estrogen on potassium-stimulated acetylcholine release in the hippocampus and overlying cortex of adult rats. Brain Res. 749:1997;143-146.
14. Gibbs R.B., Wu D., Hersh L.B., Pfaff D.W. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol. 129:1994;70-80.
15. Gibbs R.B., Pfaff D.W. In situ hybridization detection of trkA mRNA in brain Distribution, colocalization with p75ngfr and up-regulation by nerve growth factor. J Comp Neurol. 341:1994;324-339.
16. NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol. 116:1992;23-29.
17. Gibbs R.B. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res. 757:1997;10-16.
18. Gibbs R.B. Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience. 101:2000;931-938.
19. Gibbs R.B. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm Behav. 42:2002;245-247.
20. Green P.S., Gordon K., Simpkins J.W. Phenolic A ring requirement for the neuroprotective effects of steroids. J Steroid Biochem Mol Biol. 63:1997;4-6.
21. Goldberg A.M., McCaman R.E. The determination of picomole amounts of acetylcholine in mammalian brain. J Neurochem. 20:1973;1-8.
22. 3H) choline high-affinity uptake in rat striatal synaptosomes. Mol Pharmacol. 9:1973;630-639.
23. Guermonprez L., Ducrocq C., Gaudry-Talarmain Y.M. Inhibition of acetylcholine synthesis and tyrosine nitration induced by peroxynitrite are differentially prevented by antioxidants. Mol Pharmacol. 60:2001;838-846.
24. Harms C., Lautenschlager M., Bergk A., Katchanov J., Freyer D., Kapinya H.U., Megow D., Dirnagl U., Weber J.R., Hortnagl H. Differential mechanisms of neuroprotection by 17 beta-estradiol in apoptotic versus necrotic neurodegeneration. J Neurosci. 21:2000;2600-2609.
25. Hebb C.O., Ling G.M., McGeer E.G., McGeer P.L., Perkins D. Effect of locally applied hemicholinium on the acetylcholine content of the caudate nucleus. Nature (Lond). 204:1964;1309-1311.
26. Ivanova T., Kuppers E., Engele J., Beyer C. Estrogen stimulates brain-derived neurotrophic factor expression in embryonic mouse midbrain neurons through a membrane-mediated and calcium-dependent mechanism. J Neurosci Res. 66:2001;221-230.
27. Jope R.S. High affinity choline transport and acetyl-CoA production in brain and their roles in the regulation of acetylcholine synthesis. Brain Res Rev. 1:1979;313-344.
28. Kar S., Issa A.M., Seto D., Auld D.S., Collier B., Quirion R. Amyloid beta-peptide inhibits high-affinity choline uptake and acetylcholine release in rat hippocampal slices. J Neurochem. 70:1998;2179-2187.
29. Knipper M., da Penha Berzaghi M., Blochl A., Breer H., Thoenen H., Lindholm D. Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur J Neurosci. 6:1994;668-671.
30. Laemmeli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
31. Lam T.-T., Leranth C. Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci. 17:2003;1997-2005.
32. Leranth C., Shanabrough M., Horvath T.L. Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience. 101:2000;349-356.
33. Luine V.N. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol. 89:1985;484-490.
34. McEwen B.S. The molecular and neuroanatomical basis for estrogen effects in the central nervous system. J Clin Endocrinol Metab. 84:1999;1790-1797.
35. McEwen B.S. Estrogens effects on the brain Multiple sites and molecular mechanisms. J Appl Physiol. 91:2001;2785-2801.
36. McEwen B.S., Akama K., Alves S., Brake W.G., Bulloch K., Lee S., Li C., Yuen G., Milner T.A. Tracking the estrogen receptor in neurons Implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA. 98:2001;7093-7100.
37. Miettinen R.A., Kalesnykas G., Koivisto E.H. Estimation of the total number of cholinergic neurons containing estrogen receptor-alpha in the rat basal forebrain. J Histochem Cytochem. 50:2002;891-902.
38. Misawa H., Nakata K., Matsuura J., Nagao M., Okuda T., Haga T. Distribution of the high-affinity choline transporter in the central nervous system of the rat. Neuroscience. 105:2001;87-89.
39. Moosmann B., Behl C. The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc Natl Acad Sci USA. 96:1999;8867-8872.
40. O'Malley C.A., Hautamaki R.D., Kelley M., Meyer E.M. Effects of ovariectomy and estradiol benzoate on high affinity choline uptake, ACh synthesis, and release from rat cerebral cortical synaptosomes. Brain Res. 403:1987;389-392.
41. Pongrac J.L., Rylett R.J. Differential effects of nerve growth factor on expression of choline acetyltransferase and sodium-coupled choline transport in basal forebrain cholinergic neurons in culture. J Neurochem. 66:1996;804-810.
42. Pongrac J.L., Rylett R.J. Optimization of serum-free culture conditions for growth of embryonic rat cholinergic basal forebrain neurons. J Neurosci Methods. 84:1998;69-76.
43. Rabbini O., Panickar K.S., Rajakumar G., King M.A., Bodor N., Meyer E.M., Simpkins J.W. 17 beta-estradiol attenuates fimbrial lesion-induced decline of ChAT-immunoreactive neurons in the rat medial septum. Exp Neurol. 146:1997;179-186.
44. Rudick C.N., Gibbs R.B., Woolley C.S. A role for the basal forebrain cholingeric system in estrogen-induced disinhibition of hippocampal pyramidal cells. J Neurosci. 23:2003;4479-4490.
45. Singh M., Meyer E.M., Millard W.J., Simpkins J.W. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res. 644:1994;305-312.
46. Singh M., Setalo 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.
47. Shughrue P.J., Scrimo P.J., Merchenthaler I. Estrogen binding and estrogen receptor characterization (ERα and ERβ) in the cholinergic neurons of the rat basal forebrain. Neuroscience. 96:2000;41-49.
48. Smith Y.R., Minoshima S., Kuhl D.E., Zubieta J.-K. Effects of long-term hormone therapy on cholinergic synaptic concentrations in healthy postmenopausal women. J Clin Endocrinol Metab. 86:2001;679-684.
49. Sohrabji F., Miranda R.C., Toran-Allerand C.D. Reciprocal regulation of estrogen and NGF-receptors by their ligands in PC12 cells. J Neurobiol. 25:1994;974-988.
50. Sommer P., Crowley H.M. Effect of steroid hormones on membrane profiles of HeLa S3 cells. Cell Biol Int. 25:2001;103-111.
51. Toran-Allerand C.D., Miranda R.C., Bentham W., Sohrabji F., Brown T.J., Hochberg R.B., MacLusky N.J. Estrogen receptors co-localize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA. 89:1992;4668-4672.
52. Towart L.A., Alves S.E., Znamensky V., Hayashi S., McEwen B.S., Milner T.A. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J Comp Neurol. 463:2003;390-401.
53. Vasudevan N., Kow L.-M., Pfaff D.W. Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc Natl Acad Sci USA. 98:2001;12267-12271.
54. Watters J.J., Campbell J.S., Cunningham M.J., Krebs E.G., Dorsa D.M. Rapid membrane effects of steroids in neuroblastoma cells Effects of estrogen on mitogen activated protein kinase signaling cascade and c-fos immediate early gene transcription. Endocrinology. 138:1997;4030-4033.
55. Whiting K.P., Restall C.J., Brain P.F. Steroid hormone-induced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci. 67:2000;743-757.
56. Williams L.R., Rylett R.J. Exogenous nerve growth factor increases the activity of high-affinity choline uptake and choline acetyltransferase in brain of Fisher 344 male rats. J Neurochem. 55:1990;1042-1049.
57. Zapata A., Capdevila J.L., Trullas R. Role of high-affinity choline uptake on extracellular choline and acetylcholine evoked by NMDA. Synapse. 35:2000;272-280.