Oestrogen synthesis in the hippocampus: Role in axon outgrowth

Journal of Neuroendocrinology

Volumn 18, Issue 11, 2006, Pages 847-856

  von Schassen, C ^a   Fester, L ^a   Prange Kiel, J ^a   Lohse, C ^a   Huber, C ^a   Bottner M ^b   Rune, Gabriele M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Aromatase; GAP 43; Neurite outgrowth; Neuroprotection; Oestrogen

Indexed keywords

AROMATASE INHIBITOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; LETROZOLE; NEUROMODULIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SMALL INTERFERING RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ESTRADIOL BLOOD LEVEL; ESTROGEN SYNTHESIS; ESTROGEN THERAPY; GENETIC TRANSFECTION; GONAD; HIPPOCAMPUS; HORMONE ACTION; METABOLIC INHIBITION; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; OVARIECTOMY; OVARY CYCLE; PRIORITY JOURNAL; PROESTRUS; PROTEIN EXPRESSION;

ANIMALS; AROMATASE; AROMATASE INHIBITORS; CELLS, CULTURED; DOWN-REGULATION; ESTRADIOL; GAP-43 PROTEIN; HIPPOCAMPUS; NEURITES; NEURONAL PLASTICITY; NITRILES; PHOSPHOPROTEINS; RATS; RNA, SMALL INTERFERING; TISSUE DISTRIBUTION; TRIAZOLES;

EID: 33749412430     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2006.01484.x     Document Type: Article

References (40)

1. Garcia-Segura LM, Azcoitia I, DonCarlos LL. Neuroprotection by estradiol. Prog Neurobiol 2001; 63: 29-60.
2. Wise PM. Estrogens and neuroprotection. Trends Endocrinol Metab 2002; 13: 229-230.
3. Bisagno V, Bowman R, Luine V. Functional aspects of estrogen in neuroprotection. Endocrine 2003; 21: 33-41.
4. Kajta M, Beyer C. Cellular strategies of estrogen-mediated neuroprotection during brain development. Endocrine 2003; 21: 3-9.
5. Saunders-Pullman R. Estrogens and Parkinson disease: Neuroprotective, symptomatic, neither, or both? Endocrine 2003; 21: 81-87.
6. Prange-Kiel J, Wehrenberg U, Jarry H, Rune GM. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 2003; 13: 226-234.
7. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, Harada N, Kimoto T, Kawato S. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 2004; 101: 865-870.
8. Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, Frotscher M, Rune GM. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 2004; 24: 5913-5921.
9. Azcoitia I, Sierra A, Veiga S, Honda S, Harada N, Garcia-Segura LM. Brain aromatase is neuroprotective. J Neurobiol 2001; 47: 318-329.
10. Azcoitia I, DonCarlos LL, Garcia-Segura LM. Estrogen and brain vulnerability. Neurotox Res 2002; 4: 235-245.
11. Veiga S, Garcia-Segura LM, Azcoitia I. Neuroprotection by the steroids pregnenolone and dehydroepiandrosterone is mediated by the enzyme aromatase. J Neurobiol 2003; 56: 398-406.
12. Brewer GJ. Isolation and culture of rat hippocampal neurons. J Neurosci Meth 1997; 71: 143-155.
13. Rune GM, Frotscher M. Neurosteroid synthesis in the hippocampus: Role in synaptic plasticity. Neuroscience 2005; 136: 833-842.
14. Sierra A. Neurosteroids: The StAR protein in the brain. J Neuroendocrinol 2004; 16: 787-793.
15. Behl C, Manthey D. Neuroprotective activities of estrogen: An update. J Neurocytol 2000; 29: 351-358.
16. Prange-Kiel J, Fester L, Zhou L, Lauke H, Carretero J, Rune GM. Inhibition of estrogen synthesis causes region-specific downregulation of synaptic protein expression in hippocampal neurons. Hippocampus 2006; in press.
17. Rune GM, Wehrenberg U, Prange-Kiel J, Zhou L, Adelmann G, Frotscher M. Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus. Neuroscience 2002; 113: 167-175.
18. Fester L, Ribeiro-Gouveia V, von Schassen C, Rune GM. Proliferation of hippocampal granule cells requires local estrogen synthesis. J Neurochem 2006; 97: 1136-1144.
19. Meiri KF, Saffell JL, Walsh FS, Doherty P. Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) phosphorylation in growth cones. J Neurosci 1998; 18: 10429-10437.
20. Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992; 12: 2549-2554.
21. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990; 10: 1286-1291.
22. Foidart A, Tlemcani O, Harada N, Abe-Dohmae S, Balthazart J. Pre- and post-translational regulation of aromatase by steroidal and non-steroidal aromatase inhibitors. Brain Res 1995; 701: 267-278.
23. Geisler J, Haynes B, Anker G, Dowsett M, Lonning PE. Influence of letrozole and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over study. J Clin Oncol 2002; 20: 751-757.
24. Thiantanawat A, Lon BJ, Brodie AM. Signaling pathway of apoptosis activated by aromatase inhibitors and antiestrogens. Cancer Res 2003; 63: 8037-8050.
25. Puddefoot JR, Barker S, Glover HR, Malouitre SDM, Vinson GP. Non-competitive steroid inhibition of estrogen receptor functions. Int J Cancer 2002; 101: 17-22.
26. Meberg PJ, Routtenberg A. Selective expression of F1/GAP-43 and PKC gene expression mRNA in pryramidal but not granule cells of the hippocampus. Neuroscience 1991; 45: 721-733.
27. McNamara RK, Routtenberg A. NMDA receptor blockade prevents kainate induction of protein F1/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fibre sprouting in the rat. Brain Res Mol Brain Res 1995; 33: 22-28.
28. Meberg PJ, Valcourt EG, Routtenberg A. Protein F/1GAP-43 gene expression patterns in hippocampus are altered 1-2 h after LTP. Brain Res Mol Brain Res 1995; 43: 343-346.
29. Cantallops I, Routtenberg A. Rapid induction by kainic acid of both axonal growth and F1/GAP-43 protein in the adult hippocampal granule cells. J Com Neurol 1996; 366: 303-319.
30. Bennowitz LI, Routtenberg A. GAP-43. an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 1997; 20: 84-91.
31. Lustig RH, Sudol M, Pfaff DW, Federoff HJ. Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Brain Res Mol Brain Res 1991; 11: 125-132.
32. Ferrini M, Bisagno V, Piroli G, Grillo C, Gonzáles Deniselle MC, De Nicola AE. Effects of estrogens on choline-acetyltransferase immunoreactivity and GAP-43 mRNA in the forebrain of young and aging male rats. Cell Mol Biol 2002; 22: 289-230.
33. Shughrue PJ, Dorsa DM. Estrogen and androgen differentially modulate the growth-associated protein GAP-43 (neuromodulin) messenger ribonucleic acid in postnatal rat brain. Endocrinology 1994; 134: 1321-1328.
34. Prevot V, Bouret S, Croix D, Alonso G, Jennes L, Mitchell V, Routtenberg A, Beauvillain JC. Growth associated protein-43 messenger ribonucleic acid expression in gonadotropin-releasing hormone neurons during the estrous cycle. Endocrinology 2000; 141: 648-1657.
35. Kadish I, van Groen T. Low levels of estrogen significantly diminish axonal sprouting after entorhinal cortex lesions in the mouse. J Neurosci 2002; 22: 4095-4102.
36. Rune GM, Lohse C, Prange-Kiel J, Fester L, Frotscher M. Synaptic plasticity in the hippocampus: Effects of estrogen from the gonads or hippocampus. Neurochem Res 2006; 31: 145-155.
37. Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, Greengard P, McEwen BS. Novel target sites for estrogen action in dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001; 142: 1284-1289.
38. Crispino M, Capano CP, Aiello A, Iannetti E, Capello A, Giuditta A. Messenger RNAs in synaptosomal fractions from rat brain. Brain Res Mol Brain Res 2001; 97: 171-176.
39. Yokomaku D, Numakawa T, Numakawa Y, Suzuki S, Matsumoto T, Adachi N, Nishio C, Taguchi T, Hatanaka H. Estrogen enhances depolarization-induced glutamate relaease through activation of phosphatidylinositol 3-kinase and mitogen-activated protein kinase in cultured hippocampal neurons. Mol Endocrinol 2003; 17: 831-844.
40. Rekart JL, Meiri K, Routtenberg A. Hippocampal-dependent memory is impaired in heterozygous GAP-43 knock-out mice. Hippocampus 2005; 15: 1-7.