Oestrogens and neurogenesis: New functions for an old hormone. Lessons from the zebrafish;OEstrogènes et neurogenèse: de nouvelles fonctions pour une vieille hormone. Leçons tirèes du poisson zèbre

Journal de la Societe de Biologie

Volumn 203, Issue 1, 2009, Pages 29-38

  Kah, Olivier ^a   Pellegrini, Elisabeth ^a   Mouriec, Karen ^a   Diotel, Nicolas ^a   Anglade, Isabelle ^a   Vaillant, Colette ^a   Thieulant, Marie Lise ^a   Tong, Sok Keng ^b   Brion, François ^c   Chung, Bon Chu ^b   Pakdel, Farzad ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c INSTITUT NATIONAL DE L ENVIRONNEMENT INDUSTRIEL ET DES RISQUES INERIS   (France)

Author keywords

Aromatase; Astrocyte; Estradiol; Neurogenesis; Radial glial cell

Indexed keywords

AVES; DANIO RERIO; MAMMALIA; TELEOSTEI; VERTEBRATA;

AROMATASE; CYP19A PROTEIN, ZEBRAFISH; CYP19B PROTEIN, ZEBRAFISH; ESTROGEN; NERVE PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL; BIOSYNTHESIS; BIRD; BRAIN; CELL DIVISION; COMPARATIVE STUDY; CYTOLOGY; ENZYMOLOGY; GENETICS; GLIA; MAMMAL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; REGENERATION; REVIEW; SPECIES DIFFERENCE; STEM CELL; ZEBRA FISH;

ANIMALS; AROMATASE; BIRDS; BRAIN; CELL DIVISION; ESTROGENS; MAMMALS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEUROGLIA; NEURONS; REGENERATION; SPECIES SPECIFICITY; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77952317825     PISSN: 12950661     EISSN: None     Source Type: Journal    
DOI: 10.1051/jbio:2009007     Document Type: Article

References (61)

1. Adolf B., Chapouton P., Lam C.S., Topp S., Tannhauser B., Strahle U., Gotz M., Bally-Cuif L. Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol, 2006, 295, 278-293.
2. Anthony T.E., Mason H.A., Gridley T., Fishell G., Heintz N. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev, 2005, 19, 1028-1033.
3. Azcoitia I., Sierra A., Veiga S., Garcia-Segura L.M. Aromatase expression by reactive astroglia is neuroprotective. Ann N Y Acad Sci, 2003, 1007, 298-305.
4. Balthazart J., Ball G.F. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci, 1998, 21, 243-249.
5. Bentivoglio M., Mazzarello P. The history of radial glia. Brain Res Bull, 1999, 49, 305-315.
6. Bulun S.E., Takayama K., Suzuki T., Sasano H., Yilmaz B., Sebastian S. Organization of the human aromatase p450 (CYP19) gene. Semin Reprod Med, 2004, 22, 5-9.
7. Callard G.V., Petro Z., Ryan K.J. Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology, 1978, 103, 2283-2290.
8. Chapouton P., Jagasia R., Bally-Cuif L. Adult neurogenesis in non-mammalian vertebrates. Bioessays, 2007, 29, 745-757.
9. de Lacalle S. Estrogen effects on neuronal morphology. Endocrine, 2006, 29, 185-190.
10. Ekstrom P., Johnsson C.M., Ohlin L.M. Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones. J Comp Neurol, 2001, 436, 92-110.
11. Farage M.A., Osborn T.W., MacLean A.B. Cognitive, sensory, and emotional changes associated with the menstrual cycle: a review. Arch Gynecol Obstet, 2008, 278, 299-307.
12. Forlano P.M., Deitcher D.L., Myers D.A., Bass A.H. Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci, 2001, 21, 8943-8955.
13. Galea L.A. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev, 2008, 57, 332-341.
14. Ganat Y., Soni S., Chacon M., Schwartz M.L., Vaccarino F.M. Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience, 2002, 112, 977-991.
15. Garcia-Ovejero D., Azcoitia I., Doncarlos L.L., Melcangi R.C., Garcia-Segura L.M. Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res Brain Res Rev, 2005, 48, 273-286.
16. Garcia-Segura L.M. Aromatase in the brain: not just for reproduction anymore. J Neuroendocrinol, 2008, 20, 705-712.
17. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat Rev Mol Cell Biol, 2005, 6, 777-788.
18. Grandel H., Kaslin J., Ganz J., Wenzel I., Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: Origin, proliferation dynamics, migration and cell fate. Dev Biol, 2006, 295, 263-277.
19. Hojo Y., Murakami G., Mukai H., Higo S., Hatanaka Y., Ogiue-Ikeda M., Ishii H., Kimoto T., Kawato S. Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol Cell Endocrinol, 2008, 290, 31-43.
20. Kallivretaki E., Eggen R.I., Neuhauss S.C., Kah O., Segner H. The zebrafish, brain-specific, aromatase cyp19a2 is neither expressed nor distributed in a sexually dimorphic manner during sexual differentiation. Dev Dyn, 2007, 236, 3155-3166.
21. Kelly M.J., Ronnekleiv O.K. Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol, 2008, 290, 14-23.
22. Kirsche W. On postembryonic matrix zones in the brain of various vertebrates and their relationship to the study of the brain structure. Z Mikrosk Anat Forsch, 1967, 77, 313-406.
23. Kranz D., Richter W. Autoradiographic studies on the localization of the matrix zones of the diencephalon of young and adult Lebistes reticulatus (Teleostae). Z Mikrosk Anat Forsch, 1970a, 82, 42-66.
24. Kranz D., RichterW. Autoradiographic studies on the synthesis of DNA in the cerebellum and medulla oblongata of teleosts of various ages. Z Mikrosk Anat Forsch, 1970b, 82, 264-292.
25. Le Page Y., Menuet A., Kah O., Pakdel F. Characterization of a cis-acting element involved in cell-specific expression of the zebrafish brain aromatase gene. Mol Reprod Dev, 2008, 75, 1549-1557.
26. Le Page Y., Scholze M., Kah O., Pakdel F. Assessment of xenoestrogens using three distinct estrogen receptors and the zebrafish brain aromatase gene in a highly responsive glial cell system. Environ Health Perspect, 2006, 114, 752-758.
27. Lephart E.D. A review of brain aromatase cytochrome P450. Brain Res Brain Res Rev, 1996, 22, 1-26.
28. Lindsey B.W., Tropepe V. A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol, 2006, 80, 281-307.
29. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci, 2006, 7, 179-193.
30. Luine V.N. Sex steroids and cognitive function. J Neuroendocrinol, 2008, 20, 866-872.
31. Martinez-Cerdeno V., Noctor S.C., Kriegstein A.R. Estradiol stimulates progenitor cell division in the ventricular and subventricular zones of the embryonic neocortex. Eur J Neurosci, 2006, 24, 3475-3488.
32. Menuet A., Anglade I., Le Guevel R., Pellegrini E., Pakdel F., Kah O. Distribution of aromatase mRNA and protein in the brain and pituitary of female rainbow trout: Comparison with estrogen receptor alpha. J Comp Neurol, 2003, 462, 180-193.
33. Menuet A., Pellegrini E., Brion F., Gueguen M.M., Anglade I., Pakdel F., Kah O. Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene. J Comp Neurol, 2005, 485, 304-320.
34. Micevych P.E., Mermelstein P.G. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol, 2008, 38, 66-77.
35. Mouriec K., Pellegrini E., Anglade I., Menuet A., Adrio F., Thieulant M.L., Pakdel F., Kah O. Synthesis of estrogens in progenitor cells of adult fish brain: evolutive novelty or exaggeration of a more general mechanism implicating estrogens in neurogenesis ? Brain Res Bull, 2008, 75, 274-280.
36. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci, 2002, 22, 3161-3173.
37. Noctor S.C., Martinez-Cerdeno V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci, 2004, 7, 136-144.
38. Pasmanik M., Callard G.V. Aromatase and 5 alphareductase in the teleost brain, spinal cord, and pituitary gland. Gen Comp Endocrinol, 1985, 60, 244-251.
39. Pellegrini E., Menuet A., Lethimonier C., Adrio F., Gueguen M.M., Tascon C., Anglade I., Pakdel F., Kah O. Relationships between aromatase and estrogen receptors in the brain of teleost fish. Gen Comp Endocrinol, 2005, 142, 60-66.
40. Pellegrini E., Mouriec K., Anglade I., Menuet A., Le Page Y., Gueguen M.M., Marmignon M.H., Brion F., Pakdel F., Kah O. Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish. J Comp Neurol, 2007, 501, 150-167.
41. Peterson R.S., Lee D.W., Fernando G., Schlinger B.A. Radial glia express aromatase in the injured zebra finch brain. J Comp Neurol, 2004, 475, 261-269.
42. Raz L., Khan M.M., Mahesh V.B., Vadlamudi R.K., Brann D.W. Rapid estrogen signaling in the brain. Neurosignals, 2008, 16, 140-153.
43. Safe S. Environmental estrogens: roles in male reproductive tract problems and in breast cancer. Rev Environ Health, 2002, 17, 253-262.
44. Saravia F., Beauquis J., Pietranera L., De Nicola A.F. Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology, 2007, 32, 480-492.
45. Sharif A., Legendre P., Prevot V., Allet C., Romao L., Studler J.M., Chneiweiss H., Junier M.P. Transforming growth factor alpha promotes sequential conversion of mature astrocytes into neural progenitors and stem cells. Oncogene, 2007, 26, 2695-2706.
46. Siegel N., Hoegg S., Salzburger W., Braasch I., Meyer A. Comparative genomics of ParaHox clusters of teleost fishes: gene cluster breakup and the retention of gene sets following whole genome duplications. BMC Genomics, 2007, 8, 312.
47. Simpkins J.W., Singh M. More than a decade of estrogen neuroprotection. Alzheimers Dement, 2008, 4, S131-136.
48. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol, 2008, 29, 219-237.
49. Suzuki S., Gerhold L.M., Bottner M., Rau S.W., Dela Cruz C., Yang E., Zhu H., Yu J., Cashion A.B., Kindy M.S., Merchenthaler I., Gage F.H., Wise P.M. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol, 2007, 500, 1064-1075.
50. Tchoudakova A., Callard G.V. Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology, 1998, 139, 2179-2189.
51. Tchoudakova A., Kishida M., Wood E., Callard G.V. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J Steroid Biochem Mol Biol, 2001, 78, 427-439.
52. Tong S.K., Mouriec K., Kuo M.W., Pellegrini E., Gueguen M.M., Brion F., Kah O., Chung B.C., 2009. A cyp19a1b-GFP (Aromatase B) transgenic zebrafish line that expresses GFP in radial glial cells. Genesis, in press.
53. Toran-Allerand C.D. Estrogen and the brain: beyond ERalpha, ER-beta, and 17beta-estradiol. Ann N Y Acad Sci, 2005, 1052, 136-144.
54. Vaccarino F.M., Fagel D.M., Ganat Y., Maragnoli M.E., Ment L.R., Ohkubo Y., Schwartz M.L., Silbereis J., Smith K.M. Astroglial cells in development, regeneration, and repair. Neuroscientist, 2007, 13, 173-185.
55. Walf A.A., Frye C.A. Rapid and estrogen receptor beta mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids, 2008, 73, 997-1007.
56. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol, 2007, 47, 657-680.
57. Yague J.G., Munoz A., de Monasterio-Schrader P., Defelipe J., Garcia-Segura L.M., Azcoitia I. Aromatase expression in the human temporal cortex. Neuroscience, 2006, 138, 389-401.
58. Zhang R.L., Zhang Z.G., Chopp M. Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology, 2008, 55, 345-352.
59. Zupanc G.K. Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 2006, 192, 649-670.
60. Zupanc G.K., Hinsch K., Gage F.H. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol, 2005, 488, 290-319.
61. Zupanc G.K., Zupanc M.M. New neurons for the injured brain: mechanisms of neuronal regeneration in adult teleost fish. Regen Med, 2006, 1, 207-216.