Effects of estradiol in adult neurogenesis and brain repair in zebrafish

Hormones and Behavior

Volumn 63, Issue 2, 2013, Pages 193-207

  Diotel, Nicolas ^a   Vaillant, Colette ^a   Gabbero, Cyril ^a   Mironov, Svetlana ^a   Fostier, Alexis ^a   Gueguen, Marie Madeleine ^a   Anglade, Isabelle ^a   Kah, Olivier ^a   Pellegrini, Elisabeth ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Aromatase B; Brain repair; Estrogen; Lesion; Neurogenesis; Radial glial cells; Teleost; Zebrafish

Indexed keywords

AROMATASE; AROMATASE B; CASPASE 3; ESTRADIOL; ESTROGEN RECEPTOR; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; BRAIN FUNCTION; BRAIN INJURY; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; GLIA CELL; IMMUNOHISTOCHEMISTRY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA EXTRACTION; TELENCEPHALON; TELEOST; UPREGULATION; ZEBRA FISH;

ADULT STEM CELLS; AGE FACTORS; ANIMALS; BRAIN INJURIES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ESTRADIOL; MALE; MODELS, BIOLOGICAL; NERVE REGENERATION; NEUROGENESIS; PROSENCEPHALON; WOUND HEALING; ZEBRAFISH;

EID: 84872843126     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.04.003     Document Type: Review

References (99)

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. Alkayed N.J., Goto S., Sugo N., Joh H.D., Klaus J., Crain B.J., Bernard O., Traystman R.J., Hurn P.D. Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. J. Neurosci. 2001, 21:7543-7550.
3. Ayari B., El Hachimi K.H., Yanicostas C., Landoulsi A., Soussi-Yanicostas N. Prokineticin 2 expression is associated with neural repair of injured adult zebrafish telencephalon. J. Neurotrauma 2010, 27:959-972.
4. Azcoitia I., Sierra A., Veiga S., Honda S., Harada N., Garcia-Segura L.M. Brain aromatase is neuroprotective. J. Neurobiol. 2001, 47:318-329.
5. 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.
6. Barha C.K., Galea L.A. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1056-1067.
7. Baumgart E.V., Barbosa J.S., Bally-Cuif L., Gotz M., Ninkovic J. Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 2011, 60:343-357.
8. Bazer F.W., Wu G., Spencer T.E., Johnson G.A., Burghardt R.C., Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol. Hum. Reprod. 2010, 16:135-152.
9. Becker C.G., Becker T. Adult zebrafish as a model for successful central nervous system regeneration. Restor. Neurol. Neurosci. 2008, 26:71-80.
10. Boonyaratanakornkit V., McGowan E., Sherman L., Mancini M.A., Cheskis B.J., Edwards D.P. The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol. Endocrinol. 2007, 21:359-375.
11. Bowers J.M., Waddell J., McCarthy M.M. A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol. Biol. Sex Differ. 2010, 1:8.
12. Brinton R.D. Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol. Sci. 2009, 30:212-222.
13. Brock O., Keller M., Veyrac A., Douhard Q., Bakker J. Short term treatment with estradiol decreases the rate of newly generated cells in the subventricular zone and main olfactory bulb of adult female mice. Neuroscience 2010, 166:368-376.
14. Campbell K., Gotz M. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 2002, 25:235-238.
15. Chapouton P., Jagasia R., Bally-Cuif L. Adult neurogenesis in non-mammalian vertebrates. Bioessays 2007, 29:745-757.
16. Chapouton P., Skupien P., Hesl B., Coolen M., Moore J.C., Madelaine R., Kremmer E., Faus-Kessler T., Blader P., Lawson N.D., Bally-Cuif L. Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells. J. Neurosci. 2010, 30:7961-7974.
17. Costa M.R., Gotz M., Berninger B. What determines neurogenic competence in glia?. Brain Res. Rev. 2010, 63:47-59.
18. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
19. D'Amico L.A., Boujard D., Coumailleau P. Proliferation, migration and differentiation in juvenile and adult Xenopus laevis brains. Brain Res. 2011, 1405:31-48.
20. Diotel N., Le Page Y., Mouriec K., Tong S.K., Pellegrini E., Vaillant C., Anglade I., Brion F., Pakdel F., Chung B.C., Kah O. Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front. Neuroendocrinol. 2010, 31:172-192.
21. Diotel N., Rego J.L., Anglade I., Vaillant C., Pellegrini E., Gueguen M.M., Mironov S., Vaudry H., Kah O. Activity and expression of steroidogenic enzymes in the brain of adult zebrafish. Eur. J. Neurosci. 2011, 34:45-56.
22. Ekström 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.
23. Fan X., Warner M., Gustafsson J.A. Estrogen receptor beta expression in the embryonic brain regulates development of calretinin-immunoreactive GABAergic interneurons. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19338-19343.
24. 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.
25. Galea L.A., McEwen B.S. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 1999, 89:955-964.
26. Galea L.A., Spritzer M.D., Barker J.M., Pawluski J.L. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006, 16:225-232.
27. Galea L.A., Uban K.A., Epp J.R., Brummelte S., Barha C.K., Wilson W.L., Lieblich S.E., Pawluski J.L. Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can. J. Exp. Psychol. 2008, 62:247-260.
28. Garcia-Segura L.M. Aromatase in the brain: not just for reproduction anymore. J. Neuroendocrinol. 2008, 20:705-712.
29. Garcia-Segura L.M., Wozniak A., Azcoitia I., Rodriguez J.R., Hutchison R.E., Hutchison J.B. Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair. Neuroscience 1999, 89:567-578.
30. Gonzalez A., Piferrer F. Aromatase activity in the European sea bass (Dicentrarchus labrax L.) brain. Distribution and changes in relation to age, sex, and the annual reproductive cycle. Gen. Comp. Endocrinol. 2003, 132:223-230.
31. 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.
32. Hinfray N., Palluel O., Turies C., Cousin C., Porcher J.M., Brion F. Brain and gonadal aromatase as potential targets of endocrine disrupting chemicals in a model species, the zebrafish (Danio rerio). Environ. Toxicol. 2006, 21:332-337.
33. Horner K.C. The effect of sex hormones on bone metabolism of the otic capsule-an overview. Hear. Res. 2009, 252:56-60.
34. Jin Y., Zheng S., Fu Z. Embryonic exposure to cypermethrin induces apoptosis and immunotoxicity in zebrafish (Danio rerio). Fish Shellfish Immunol. 2011, 30:1049-1054.
35. Kah O., Pellegrini E., Mouriec K., Diotel N., Anglade I., Vaillant C., Thieulant M.L., Tong S.K., Brion F., Chung B.C., Pakdel F. Oestrogens and neurogenesis: new functions for an old hormone. Lessons from the zebrafish. J. Soc. Biol. 2009, 203:29-38.
36. Karasu T., Marczylo T.H., Maccarrone M., Konje J.C. The role of sex steroid hormones, cytokines and the endocannabinoid system in female fertility. Hum. Reprod. Update 2011, 17:347-361.
37. Kishimoto N., Shimizu K., Sawamoto K. Neuronal regeneration in a zebrafish model of adult brain injury. Dis. Model. Mech. 2011, 5:200-209.
38. Kizil C., Kaslin J., Kroehne V., Brand M. Adult neurogenesis and brain regeneration in zebrafish. Dev. Neurobiol. 2011, 72:429-461.
39. Kroehne V., Freudenreich D., Hans S., Kaslin J., Brand M. Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development. 2011, 138(22):4831-4841. Epub 2011 Oct 17.
40. Lam C.S., Marz M., Strahle U. gfap and nestin reporter lines reveal characteristics of neural progenitors in the adult zebrafish brain. Dev. Dyn. 2009, 238:475-486.
41. 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.
42. Le Page Y., Diotel N., Vaillant C., Pellegrini E., Anglade I., Merot Y., Kah O. Aromatase, brain sexualization and plasticity: the fish paradigm. Eur. J. Neurosci. 2010, 32:2105-2115.
43. Le Roux P.D., Reh T.A. Regional differences in glial-derived factors that promote dendritic outgrowth from mouse cortical neurons in vitro. J. Neurosci. 1994, 14:4639-4655.
44. Lephart E.D. A review of brain aromatase cytochrome P450. Brain Res. Brain Res. Rev. 1996, 22:1-26.
45. Li J., Siegel M., Yuan M., Zeng Z., Finnucan L., Persky R., Hurn P.D., McCullough L.D. Estrogen enhances neurogenesis and behavioral recovery after stroke. J. Cereb. Blood Flow Metab. 2011, 31:413-425.
46. Lindsey B.W., Tropepe V. A comparative framework for understanding the biological principles of adult neurogenesis. Prog. Neurobiol. 2006, 80:281-307.
47. Liu X., Fan X.L., Zhao Y., Luo G.R., Li X.P., Li R., Le W.D. Estrogen provides neuroprotection against activated microglia-induced dopaminergic neuronal injury through both estrogen receptor-alpha and estrogen receptor-beta in microglia. J. Neurosci. Res. 2005, 81:653-665.
48. 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. 2011, 38:577-585.
49. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
50. 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.
51. März M., Chapouton P., Diotel N., Vaillant C., Hesl B., Takamiya M., Lam C.S., Kah O., Bally-Cuif L., Strahle U. Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon. Glia 2010, 58:870-888.
52. März M., Schmidt R., Rastegar S., Strahle U. Regenerative response following stab injury in the adult zebrafish telencephalon. Dev. Dyn. 2011, 240:2221-2231.
53. Matthews J., Gustafsson J.A. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol. Interv. 2003, 3:281-292.
54. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., Galea L.A. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 2006, 141:1793-1800.
55. McCarthy M.M. The two faces of estradiol: effects on the developing brain. Neuroscientist 2009, 15:599-610.
56. McEwen B.S., Gould E., Orchinik M., Weiland N.G., Woolley C.S. Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes. Ciba Found Symp 191 1995, 52-66. discussion 66-73.
57. 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.
58. 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.
59. Mesiano S., Wang Y., Norwitz E.R. Progesterone receptors in the human pregnancy uterus: do they hold the key to birth timing?. Reprod. Sci. 2011, 18:6-19.
60. Mouriec K., Gueguen M.M., Manuel C., Percevault F., Thieulant M.L., Pakdel F., Kah O. Androgens upregulate cyp19a1b (aromatase B) gene expression in the brain of zebrafish (Danio rerio) through estrogen receptors. Biol. Reprod. 2009, 80:889-896.
61. Murakami G., Tsurugizawa T., Hatanaka Y., Komatsuzaki Y., Tanabe N., Mukai H., Hojo Y., Kominami S., Yamazaki T., Kimoto T., Kawato S. Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus. Biochem. Biophys. Res. Commun. 2006, 351:553-558.
62. Murashov A.K., Pak E.S., Hendricks W.A., Tatko L.M. 17beta-Estradiol enhances neuronal differentiation of mouse embryonic stem cells. FEBS Lett. 2004, 569:165-168.
63. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
64. 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.
65. Ormerod B.K., Galea L.A. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 2001, 102:369-379.
66. Ormerod B.K., Lee T.T., Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 2003, 55:247-260.
67. Ormerod B.K., Lee T.T., Galea L.A. Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons. Neuroscience 2004, 128:645-654.
68. Pawluski J.L., Brummelte S., Barha C.K., Crozier T.M., Galea L.A. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol. 2009, 30:343-357.
69. 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.
70. Peterson R.S., Saldanha C.J., Schlinger B.A. Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 2001, 13:317-323.
71. 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.
72. Pettersson K., Gustafsson J.A. Role of estrogen receptor beta in estrogen action. Annu. Rev. Physiol. 2001, 63:165-192.
73. Phoenix C.H., Goy R.W., Gerall A.A., Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
74. Rothenaigner I., Krecsmarik M., Hayes J.A., Bahn B., Lepier A., Fortin G., Gotz M., Jagasia R., Bally-Cuif L. Clonal analysis by distinct viral vectors identifies bona fide neural stem cells in the adult zebrafish telencephalon and characterizes their division properties and fate. Development 2011, 138:1459-1469.
75. Rowitch D.H., Kriegstein A.R. Developmental genetics of vertebrate glial-cell specification. Nature 2010, 468:214-222.
76. Saldanha C.J., Duncan K.A., Walters B.J. Neuroprotective actions of brain aromatase. Front. Neuroendocrinol. 2009, 30:106-118.
77. 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.
78. Sasaki T., Kitagawa K., Yagita Y., Sugiura S., Omura-Matsuoka E., Tanaka S., Matsushita K., Okano H., Tsujimoto Y., Hori M. Bcl2 enhances survival of newborn neurons in the normal and ischemic hippocampus. J. Neurosci. Res. 2006, 84:1187-1196.
79. Simpson E.R., Davis S.R. Minireview: aromatase and the regulation of estrogen biosynthesis-some new perspectives. Endocrinology 2001, 142:4589-4594.
80. Smith C.C., Vedder L.C., McMahon L.L. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 2009, 34(Suppl. 1):S130-S142.
81. Strobl-Mazzulla P.H., Lethimonier C., Gueguen M.M., Karube M., Fernandino J.I., Yoshizaki G., Patino R., Strussmann C.A., Kah O., Somoza G.M. Brain aromatase (Cyp19A2) and estrogen receptors, in larvae and adult pejerrey fish Odontesthes bonariensis: neuroanatomical and functional relations. Gen. Comp. Endocrinol. 2008, 158:191-201.
82. 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.
83. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 1999, 19:5792-5801.
84. 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.
85. Thompson C.K. Cell death and the song control system: a model for how sex steroid hormones regulate naturally-occurring neurodegeneration. Dev. Growth Differ. 2011, 53:213-224.
86. Tong S.K., Mouriec K., Kuo M.W., Pellegrini E., Gueguen M.M., Brion F., Kah O., Chung B.C. A cyp19a1b-gfp (aromatase B) transgenic zebrafish line that expresses GFP in radial glial cells. Genesis 2009, 47:67-73.
87. Tsukahara S. Sex differences and the roles of sex steroids in apoptosis of sexually dimorphic nuclei of the preoptic area in postnatal rats. J. Neuroendocrinol. 2009, 21:370-376.
88. Tsurugizawa T., Mukai H., Tanabe N., Murakami G., Hojo Y., Kominami S., Mitsuhashi K., Komatsuzaki Y., Morrison J.H., Janssen W.G., Kimoto T., Kawato S. Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 2005, 337:1345-1352.
89. Valencia C.A., Bailey C., Liu R. Novel zebrafish caspase-3 substrates. Biochem. Biophys. Res. Commun. 2007, 361:311-316.
90. Wang L., Andersson S., Warner M., Gustafsson J.A. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2792-2796.
91. Wang L., Andersson S., Warner M., Gustafsson J.A. Estrogen receptor (ER)beta knockout mice reveal a role for ERbeta in migration of cortical neurons in the developing brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:703-708.
92. Wang X., Tsai J.W., Lamonica B., Kriegstein A.R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 2011, 14:555-561.
93. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 2007, 47:657-680.
94. Wullimann M.F., Rupp B., Reichert H. Neuroanatomy of the zebrafish brain. A Topological Atlas 1996, 1-144. Birhaüser Verlag, Basel, Switzerland.
95. Wynne R.D., Walters B.J., Bailey D.J., Saldanha C.J. Inhibition of injury-induced glial aromatase reveals a wave of secondary degeneration in the songbird brain. Glia 2008, 56:97-105.
96. Zakar T., Mesiano S. How does progesterone relax the uterus in pregnancy?. N. Engl. J. Med. 2011, 364:972-973.
97. Zupanc G.K. Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav. Evol. 2001, 58:250-275.
98. Zupanc G.K. Towards brain repair: insights from teleost fish. Semin. Cell Dev. Biol. 2009, 20:683-690.
99. 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.