Aromatase, estrogen receptors and brain development in fish and amphibians

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 2, 2015, Pages 152-162

  Coumailleau, Pascal ^a   Pellegrini, Elisabeth ^a   Adrio, Fátima ^b   Diotel, Nicolas ^c   Cano Nicolau, Joel ^a   Nasri, Ahmed ^a   Vaillant, Colette ^a   Kah, Olivier ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^c Groupe d'Etude sur l'Inflammation Chronique et l'Obésité GEICO EA 4516 Faculté des Sciences et Technologies   (France)

Author keywords

Aromatase; Estrogen receptor; Neurogenesis; Radial glia; Xenopus laevis; Zebrafish

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AROMATASE; CELL NUCLEUS RECEPTOR; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; GONADORELIN; MESSENGER RNA;

AMPHIBIA; BRAIN DEVELOPMENT; CELL MIGRATION; CELL PROLIFERATION; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FISH; GENE EXPRESSION; GLIA; MACROGLIA; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TELEOST; UPREGULATION; ANIMAL; ANIMAL EMBRYO; BRAIN; DRUG EFFECTS; EMBRYOLOGY; GENETICS; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; ZEBRA FISH;

AMPHIBIA; ANIMALIA; ANURA; DANIO RERIO; TELEOSTEI; VERTEBRATA; XENOPUS LAEVIS;

AMPHIBIANS; ANIMALS; AROMATASE; BRAIN; EMBRYO, NONMAMMALIAN; ENDOCRINE DISRUPTORS; FISHES; NEUROGENESIS; NEUROGLIA; RECEPTORS, ESTROGEN; ZEBRAFISH;

EID: 84921051575     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.07.002     Document Type: Review

References (177)

1. Doisy E.A., Thayer S.A. The oestrus-producing hormones. Science 1932, 75:216-217.
2. Zondek B. Estrogenic hormone in the urine of the stallion. Nature 1934, 133:209-210.
3. 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.
4. Azcoitia I., Yague J.G., Garcia-Segura L.M. Estradiol synthesis within the human brain. Neuroscience 2011, 191:139-147.
5. Garcia-Segura L.M. Aromatase in the brain: not just for reproduction anymore. J. Neuroendocrinol. 2008, 20:705-712.
6. Lephart E.D. A review of brain aromatase cytochrome P450. Brain Res. Brain Res. Rev. 1996, 22:1-26.
7. Jost A. Hormonal factors in the sex differentiation of the mammalian foetus. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1970, 259:119-130.
8. MacLusky N.J., Philip A., Hurlburt C., Naftolin F. Estrogen formation in the developing rat brain: sex differences in aromatase activity during early post-natal life. Psychoneuroendocrinology 1985, 10:355-361.
9. Simerly R.B. Wired on hormones: endocrine regulation of hypothalamic development. Curr. Opin. Neurobiol. 2005, 15:81-85.
10. Waters E.M., Simerly R.B. Estrogen induces caspase-dependent cell death during hypothalamic development. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:9714-9718.
11. Gillies G.E., McArthur S. Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol. Rev. 2010, 62:155-198.
12. Bayer J., Rune G., Kutsche K., Schwarze U., Kalisch R., Buchel C., Sommer T. Estrogen and the male hippocampus: genetic variation in the aromatase gene predicting serum estrogen is associated with hippocampal gray matter volume in men. Hippocampus 2013, 23:117-121.
13. 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.
14. Bredemann T.M., McMahon L.L. 17Beta estradiol increases resilience and improves hippocampal synaptic function in helpless ovariectomized rats. Psychoneuroendocrinology 2014, 42:77-88.
15. Suzuki S., Brown C.M., Wise P.M. Neuroprotective effects of estrogens following ischemic stroke. Front. Neuroendocrinol. 2009, 30:201-211.
16. Waddell J., Bowers J.M., Edwards N.S., Jordan C.L., McCarthy M.M. Dysregulation of neonatal hippocampal cell genesis in the androgen insensitive Tfm rat. Horm. Behav. 2013, 64:144-152.
17. Czajka-Oraniec I., Simpson E.R. Aromatase research and its clinical significance. Endokrynol. Pol. 2010, 61:126-134.
18. De Nicola A.F., Brocca M.E., Pietranera L., Garcia-Segura L.M. Neuroprotection and sex steroid hormones: evidence of estradiol-mediated protection in hypertensive encephalopathy. Mini Rev. Med. Chem. 2012, 12:1081-1089.
19. Filova B., Ostatnikova D., Celec P., Hodosy J. The effect of testosterone on the formation of brain structures. Cells Tissues Organs 2013, 197:169-177.
20. Remage-Healey L., Saldanha C.J., Schlinger B.A. Estradiol synthesis and action at the synapse: evidence for "synaptocrine" signaling. Front. Endocrinol. 2011, 2:28.
21. Saldanha C.J., Burstein S.R., Duncan K.A. Induced synthesis of oestrogens by glia in the songbird brain. J. Neuroendocrinol. 2013, 25:1032-1038.
22. Saldanha C.J., Duncan K.A., Walters B.J. Neuroprotective actions of brain aromatase. Front. Neuroendocrinol. 2009, 30:106-118.
23. 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.
24. Luchetti S., van Eden C.G., Schuurman K., van Strien M.E., Swaab D.F., Huitinga I. Gender differences in multiple sclerosis: induction of estrogen signaling in male and progesterone signaling in female lesions. J. Neuropathol. Exp. Neurol. 2014, 73:123-135.
25. Peterson R.S., Fernando G., Day L., Allen T.A., Chapleau J.D., Menjivar J., Schlinger B.A., Lee D.W. Aromatase expression and cell proliferation following injury of the adult zebra finch hippocampus. Dev. Neurobiol. 2007, 67:1867-1878.
26. 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.
27. 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.
28. Spence R.D., Zhen Y., White S., Schlinger B.A., Day L.B. Recovery of motor and cognitive function after cerebellar lesions in a songbird: role of estrogens. Eur. J. Neurosci. 2009, 29:1225-1234.
29. Balthazart J., Absil P., Foidart A., Houbart M., Harada N., Ball G.F. Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol. 1996, 31:129-148.
30. Balthazart J., Ball G.F. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci. 1998, 21:243-249.
31. Campbell C.M., Fostier A., Jalabert B., Truscott B. Identification and quantification of steroids in the serum of rainbow trout during spermiation and oocyte maturation. J. Endocrinol. 1980, 85:371-378.
32. Scott A.P., Sumpter J.P., Hardiman P.A. Hormone changes during ovulation in the rainbow trout (Salmo gairdneri Richardson). Gen. Comp. Endocrinol. 1983, 49:128-134.
33. Godwin J. Neuroendocrinology of sexual plasticity in teleost fishes. Front. Neuroendocrinol. 2010, 31:203-216.
34. Steinke D., Hoegg S., Brinkmann H., Meyer A. Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol. 2006, 4:16.
35. Pakdel F., Feon S., Le Gac F., Le Menn F., Valotaire Y. In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol. Cell. Endocrinol. 1991, 75:205-212.
36. Pakdel F., Le Gac F., Le Goff P., Valotaire Y. Full-length sequence and in vitro expression of rainbow trout estrogen receptor cDNA. Mol. Cell. Endocrinol. 1990, 71:195-204.
37. Green S., Walter P., Kumar V., Krust A., Bornert J.M., Argos P., Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 1986, 320:134-139.
38. Metivier R., Petit F.G., Valotaire Y., Pakdel F. Function of N-terminal transactivation domain of the estrogen receptor requires a potential alpha-helical structure and is negatively regulated by the A domain. Mol. Endocrinol. 2000, 14:1849-1871.
39. Pakdel F., Metivier R., Flouriot G., Valotaire Y. Two estrogen receptor (ER) isoforms with different estrogen dependencies are generated from the trout ER gene. Endocrinology 2000, 141:571-580.
40. Menuet A., Anglade I., Flouriot G., Pakdel F., Kah O. Tissue-specific expression of two structurally different estrogen receptor alpha isoforms along the female reproductive axis of an oviparous species, the rainbow trout. Biol. Reprod. 2001, 65:1548-1557.
41. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:5925-5930.
42. Hawkins M.B., Thornton J.W., Crews D., Skipper J.K., Dotte A., Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10751-10756.
43. Menuet A., Pellegrini E., Anglade I., Blaise O., Laudet V., Kah O., Pakdel F. Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol. Reprod. 2002, 66:1881-1892.
44. Salbert G., Bonnec G., Le Goff P., Boujard D., Valotaire Y., Jego P. Localization of the estradiol receptor mRNA in the forebrain of the rainbow trout. Mol. Cell. Endocrinol. 1991, 76:173-180.
45. Anglade I., Pakdel F., Bailhache T., Petit F., Salbert G., Jego P., Valotaire Y., Kah O. Distribution of estrogen receptor-immunoreactive cells in the brain of the rainbow trout (Oncorhynchus mykiss). J. Neuroendocrinol. 1994, 6:573-583.
46. Pakdel F., Petit F., Anglade I., Kah O., Delaunay F., Bailhache T., Valotaire Y. Overexpression of rainbow trout estrogen receptor domains in Escherichia coli: characterization and utilization in the production of antibodies for immunoblotting and immunocytochemistry. Mol. Cell. Endocrinol. 1994, 104:81-93.
47. 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.
48. 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.
49. Muriach B., Carrillo M., Zanuy S., Cerda-Reverter J.M. Distribution of estrogen receptor 2 mRNAs (Esr2a and Esr2b) in the brain and pituitary of the sea bass (Dicentrarchus labrax). Brain Res. 2008, 1210:126-141.
50. Muriach B., Cerda-Reverter J.M., Gomez A., Zanuy S., Carrillo M. Molecular characterization and central distribution of the estradiol receptor alpha (ERalpha) in the sea bass (Dicentrarchus labrax). J. Chem. Neuroanat. 2008, 35:33-48.
51. Kanda S., Akazome Y., Mitani Y., Okubo K., Oka Y. Neuroanatomical evidence that kisspeptin directly regulates isotocin and vasotocin neurons. PLoS One 2013, 8:e62776.
52. Zempo B., Kanda S., Okubo K., Akazome Y., Oka Y. Anatomical distribution of sex steroid hormone receptors in the brain of female medaka. J. Comp. Neurol. 2013, 521:1760-1780.
53. Linard B., Anglade I., Corio M., Navas J.M., Pakdel F., Saligaut C., Kah O. Estrogen receptors are expressed in a subset of tyrosine hydroxylase-positive neurons of the anterior preoptic region in the rainbow trout. Neuroendocrinology 1996, 63:156-165.
54. Anglade I., Mazurais D., Douard V., Le Jossic-Corcos C., Mananos E.L., Michel D., Kah O. Distribution of glutamic acid decarboxylase mRNA in the forebrain of the rainbow trout as studied by in situ hybridization. J. Comp. Neurol. 1999, 410:277-289.
55. Mitani Y., Kanda S., Akazome Y., Zempo B., Oka Y. Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Endocrinology 2010, 151:1751-1759.
56. Escobar S., Felip A., Gueguen M.M., Zanuy S., Carrillo M., Kah O., Servili A. Expression of kisspeptins in the brain and pituitary of the European sea bass (Dicentrarchus labrax). J. Comp. Neurol. 2013, 521:933-948.
57. 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.
58. van Nes S., Moe M., Andersen O. Molecular characterization and expression of two cyp19 (P450 aromatase) genes in embryos, larvae, and adults of Atlantic halibut (Hippoglossus hippoglossus). Mol. Reprod. Dev. 2005, 72:437-449.
59. 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. Off. J. Soc. Neurosci. 2001, 21:8943-8955.
60. 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.
61. 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.
62. Malatesta P., Gotz M. Radial glia - from boring cables to stem cell stars. Development 2013, 140:483-486.
63. Pinto L., Gotz M. Radial glial cell heterogeneity-the source of diverse progeny in the CNS. Prog. Neurobiol. 2007, 83:2-23.
64. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
65. 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.
66. D'Amico L.A., Boujard D., Coumailleau P. The neurogenic factor NeuroD1 is expressed in post-mitotic cells during juvenile and adult Xenopus neurogenesis and not in progenitor or radial glial cells. PLoS One 2013, 8:e66487.
67. Onteniente B., Kimura H., Maeda T. Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry. J. Comp. Neurol. 1983, 215:427-436.
68. 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.
69. 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.
70. Pasmanik M., Schlinger B.A., Callard G.V. In vivo steroid regulation of aromatase and 5 alpha-reductase in goldfish brain and pituitary. Gen. Comp. Endocrinol. 1988, 71:175-182.
71. Borg B., Timmers R.J., Lambert J.G. Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. I. Distribution and effects of season and photoperiod. Exp. Biol. 1987, 47:63-68.
72. Timmers R.J., Lambert J.G., Peute J., Vullings H.G., van Oordt P.G. Localization of aromatase in the brain of the male African catfish, Clarias gariepinus (Burchell), by microdissection and biochemical identification. J. Comp. Neurol. 1987, 258:368-377.
73. Borg B., Andersson E., Mayer I., Lambert J.G. Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. III. Effects of castration under different conditions and of replacement with different androgens. Exp. Biol. 1989, 48:149-152.
74. 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.
75. Forlano P.M., Bass A.H. Seasonal plasticity of brain aromatase mRNA expression in glia: divergence across sex and vocal phenotypes. J. Neurobiol. 2005, 65:37-49.
76. Jeng S.R., Yueh W.S., Pen Y.T., Gueguen M.M., Pasquier J., Dufour S., Chang C.F., Kah O. Expression of aromatase in radial glial cells in the brain of the Japanese eel provides insight into the evolution of the cyp191a gene in Actinopterygians. PLoS One 2012, 7:e44750.
77. Strobl-Mazzulla P.H., Nunez A., Pellegrini E., Gueguen M.M., Kah O., Somoza G.M. Progenitor radial cells and neurogenesis in pejerrey fish forebrain. Brain Behav. Evol. 2010, 76:20-31.
78. Okubo K., Takeuchi A., Chaube R., Paul-Prasanth B., Kanda S., Oka Y., Nagahama Y. Sex differences in aromatase gene expression in the medaka brain. J. Neuroendocrinol. 2011, 23:412-423.
79. Bentivoglio M., Mazzarello P. The history of radial glia. Brain Res. Bull. 1999, 49:305-315.
80. Garcia-Marin V., Garcia-Lopez P., Freire M. Cajal's contributions to glia research. Trends Neurosci. 2007, 30:479-487.
81. Rakic P. Neuronal migration and contact guidance in the primate telencephalon. Postgrad. Med. J. 1978, 54(Suppl. 1):25-40.
82. Xu L., Tang X., Wang Y., Xu H., Fan X. Radial glia, the keystone of the development of the hippocampal dentate gyrus. Mol. Neurobiol. 2014, in press [Epub ahead of print].
83. Morrens J., Van Den Broeck W., Kempermann G. Glial cells in adult neurogenesis. Glia 2012, 60:159-174.
84. 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.
85. George F.W., Ojeda S.R. Changes in aromatase activity in the rat brain during embryonic, neonatal, and infantile development. Endocrinology 1982, 111:522-529.
86. Lephart E.D., Simpson E.R., McPhaul M.J., Kilgore M.W., Wilson J.D., Ojeda S.R. Brain aromatase cytochrome P-450 messenger RNA levels and enzyme activity during prenatal and perinatal development in the rat. Brain Res. Mol. Brain Res. 1992, 16:187-192.
87. Borg B., Timmers R.J., Lambert J.G. Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. II. Effects of castration in winter. Exp. Biol. 1987, 47:69-71.
88. Pasmanik M., Callard G.V. Changes in brain aromatase and 5 alpha-reductase activities correlate significantly with seasonal reproductive cycles in goldfish (Carassius auratus). Endocrinology 1988, 122:1349-1356.
89. Mayer I., Borg B., Berglund I., Lambert J.G. Effects of castration and androgen treatment on aromatase activity in the brain of mature male Atlantic salmon (Salmo salar L.) parr. Gen. Comp. Endocrinol. 1991, 82:86-92.
90. Brion F., Le Page Y., Piccini B., Cardoso O., Tong S.K., Chung B.C., Kah O. Screening estrogenic activities of chemicals or mixtures in vivo using transgenic (cyp19a1b-GFP) zebrafish embryos. PLoS One 2012, 7:e36069.
91. 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.
92. 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.
93. 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. 1970, 82:42-66.
94. Kranz V.D., Richter W. Neurogenesis and regeneration in the brain of teleosts in relation to age. (Autoradiographic studies). Z. Alternsforsch. 1975, 30:371-382.
95. 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.
96. Chapouton P., Jagasia R., Bally-Cuif L. Adult neurogenesis in non-mammalian vertebrates. BioEssays 2007, 29:745-757.
97. 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. Off. J. Soc. Neurosci. 2010, 30:7961-7974.
98. 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.
99. Kaslin J., Ganz J., Geffarth M., Grandel H., Hans S., Brand M. Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:6142-6153.
100. Marz 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.
101. 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.
102. Zupanc G.K. Adult neurogenesis and neuronal regeneration in the brain of teleost fish. J. Physiol. Paris 2008, 102:357-373.
103. Diotel N., Vaillant C., Gabbero C., Mironov S., Fostier A., Gueguen M.M., Anglade I., Kah O., Pellegrini E. Effects of estradiol in adult neurogenesis and brain repair in zebrafish. Horm. Behav. 2013, 63:193-207.
104. Ampatzis K., Makantasi P., Dermon C.R. Cell proliferation pattern in adult zebrafish forebrain is sexually dimorphic. Neuroscience 2012, 226:367-381.
105. 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.
106. 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.
107. 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.
108. Garcia-Segura L.M., Naftolin F., Hutchison J.B., Azcoitia I., Chowen J.A. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J. Neurobiol. 1999, 40:574-584.
109. Pettersson K., Gustafsson J.A. Role of estrogen receptor beta in estrogen action. Annu. Rev. Physiol. 2001, 63:165-192.
110. Zupanc G.K., Sirbulescu R.F. Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Eur. J. Neurosci. 2011, 34:917-929.
111. 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 2012, 60:343-357.
112. Marz M., Schmidt R., Rastegar S., Strahle U. Regenerative response following stab injury in the adult zebrafish telencephalon. Dev. Dyn. 2011, 240:2221-2231.
113. Pellegrini E., Vaillant C., Diotel N., Benquet P., Brion F., Kah O. Expression, regulation and potential functions of aromatase in radial glial cells of the fish brain. Brain Aromatase, Estrogens, and Behavior 2013, Oxford University Press, Oxford; New York. J. Balthazart, G.F. Ball (Eds.).
114. Liu X., Zhu P., Sham K.W., Yuen J.M., Xie C., Zhang Y., Liu Y., Li S., Huang X., Cheng C.H., Lin H. Identification of a membrane estrogen receptor in zebrafish with homology to mammalian GPER and its high expression in early germ cells of the testis. Biol. Reprod. 2009, 80:1253-1261.
115. Bardet P.L., Horard B., Robinson-Rechavi M., Laudet V., Vanacker J.M. Characterization of oestrogen receptors in zebrafish (Danio rerio). J. Mol. Endocrinol. 2002, 28:153-163.
116. Chandrasekar G., Archer A., Gustafsson J.A., Andersson Lendahl M. Levels of 17beta-estradiol receptors expressed in embryonic and adult zebrafish following in vivo treatment of natural or synthetic ligands. PLoS One 2010, 5:e9678.
117. Mouriec K., Lareyre J.J., Tong S.K., Le Page Y., Vaillant C., Pellegrini E., Pakdel F., Chung B.C., Kah O., Anglade I. Early regulation of brain aromatase (cyp19a1b) by estrogen receptors during zebrafish development. Dev. Dyn. 2009, 238:2641-2651.
118. Griffin L.B., January K.E., Ho K.W., Cotter K.A., Callard G.V. Morpholino-mediated knockdown of ERalpha, ERbetaa, and ERbetab mRNAs in zebrafish (Danio rerio) embryos reveals differential regulation of estrogen-inducible genes. Endocrinology 2013, 154:4158-4169.
119. Froehlicher M., Liedtke A., Groh K., Lopez-Schier H., Neuhauss S.C., Segner H., Eggen R.I. Estrogen receptor subtype beta2 is involved in neuromast development in zebrafish (Danio rerio) larvae. Dev. Biol. 2009, 330:32-43.
120. Shi Y., Liu X., Zhu P., Li J., Sham K.W., Cheng S.H., Li S., Zhang Y., Cheng C.H., Lin H. G-protein-coupled estrogen receptor 1 is involved in brain development during zebrafish (Danio rerio) embryogenesis. Biochem. Biophys. Res. Commun. 2013, 435:21-27.
121. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., Foster P.M., Gray C.L., Gray L.E. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol. Sci. 2008, 105:235-259.
122. Cotter K.A., Yershov A., Novillo A., Callard G.V. Multiple structurally distinct ERalpha mRNA variants in zebrafish are differentially expressed by tissue type, stage of development and estrogen exposure. Gen. Comp. Endocrinol. 2013, 194:217-229.
123. Diotel N., Servili A., Gueguen M.M., Mironov S., Pellegrini E., Vaillant C., Zhu Y., Kah O., Anglade I. Nuclear progesterone receptors are up-regulated by estrogens in neurons and radial glial progenitors in the brain of zebrafish. PLoS One 2011, 6:e28375.
124. Vosges M., Kah O., Hinfray N., Chadili E., Le Page Y., Combarnous Y., Porcher J.M., Brion F. 17Alpha-ethinylestradiol and nonylphenol affect the development of forebrain GnRH neurons through an estrogen receptors-dependent pathway. Reprod. Toxicol. 2012, 33:198-204.
125. Vosges M., Le Page Y., Chung B.C., Combarnous Y., Porcher J.M., Kah O., Brion F. 17Alpha-ethinylestradiol disrupts the ontogeny of the forebrain GnRH system and the expression of brain aromatase during early development of zebrafish. Aquat. Toxicol. 2010, 99:479-491.
126. Tse W.K., Yeung B.H., Wan H.T., Wong C.K. Early embryogenesis in zebrafish is affected by bisphenol A exposure. Biol. Open 2013, 2:466-471.
127. Staples C.A., Dorn P.B., Klecka G.M., O'Block S.T., Branson D.R., Harris L.R. Bisphenol A concentrations in receiving waters near US manufacturing and processing facilities. Chemosphere 2000, 40:521-525.
128. Wang X., Dong Q., Chen Y., Jiang H., Xiao Q., Wang Y., Li W., Bai C., Huang C., Yang D. Bisphenol A affects axonal growth, musculature and motor behavior in developing zebrafish. Aquat. Toxicol. 2013, 142-143:104-113.
129. Lam S.H., Hlaing M.M., Zhang X., Yan C., Duan Z., Zhu L., Ung C.Y., Mathavan S., Ong C.N., Gong Z. Toxicogenomic and phenotypic analyses of bisphenol-A early-life exposure toxicity in zebrafish. PLoS One 2011, 6:e28273.
130. Gibert Y., Sassi-Messai S., Fini J.B., Bernard L., Zalko D., Cravedi J.P., Balaguer P., Andersson-Lendahl M., Demeneix B., Laudet V. Bisphenol A induces otolith malformations during vertebrate embryogenesis. BMC Dev. Biol. 2011, 11:4.
131. Saili K.S., Corvi M.M., Weber D.N., Patel A.U., Das S.R., Przybyla J., Anderson K.A., Tanguay R.L. Neurodevelopmental low-dose bisphenol A exposure leads to early life-stage hyperactivity and learning deficits in adult zebrafish. Toxicology 2012, 291:83-92.
132. Riu A., McCollum C.W., Pinto C.L., Grimaldi M., Hillenweck A., Perdu E., Zalko D., Bernard L., Laudet V., Balaguer P., Bondesson M., Gustafsson J.A. Halogenated bisphenol-A analogs act as obesogens in zebrafish larvae (Danio rerio). Toxicol. Sci. 2014, 139:48-58.
133. Iwabuchi J., Koshimizu K., Nakagawa T. Expression profile of the aromatase enzyme in the Xenopus brain and localization of estradiol and estrogen receptors in each tissue. Gen. Comp. Endocrinol. 2013, 194:286-294.
134. Lee J.S., Iwabuchi K., Nomaru K., Nagahama N., Kim E.Y., Iwata H. Molecular and functional characterization of a novel aryl hydrocarbon receptor isoform, AHR1beta, in the chicken (Gallus gallus). Toxicol. Sci. 2013, 136:450-466.
135. Iwabuchi J., Arai K., Miyata S. Isolation of novel isoforms of estrogen receptor genes from Xenopus gonad and brain. Zool. Sci. 2008, 25:1227-1233.
136. Fumino S., Iwai N., Deguchi E., Kimura O., Ono S., Iwabuchi T. Estrogen receptor expression in anomalous arrangement of the pancreaticobiliary duct. J. Pediatr. Surg. 2005, 40:1716-1720.
137. Takase M., Iguchi T. Molecular cloning of two isoforms of Xenopus (Silurana) tropicalis estrogen receptor mRNA and their expression during development. Biochim. Biophys. Acta 2007, 1769:172-181.
138. Wu K.H., Tobias M.L., Kelley D.B. Estrogen receptor expression in laryngeal muscle in relation to estrogen-dependent increases in synapse strength. Neuroendocrinology 2003, 78:72-80.
139. Duarte-Guterman P., Ryan M.J., Hogan N.S., Trudeau V.L. Developmental profiles and thyroid hormone regulation of brain transcripts in frogs: a species comparison with emphasis on Physalaemus pustulosus. Brain Behav. Evol. 2012, 79:98-112.
140. Chakraborty M., Burmeister S.S. Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of tungara frogs. Horm. Behav. 2010, 58:619-627.
141. Davis G.A., Moore F.L. Neuroanatomical distribution of androgen and estrogen receptor-immunoreactive cells in the brain of the male roughskin newt. J. Comp. Neurol. 1996, 372:294-308.
142. Guerriero G., Roselli C.E., Paolucci M., Botte V., Ciarcia G. Estrogen receptors and aromatase activity in the hypothalamus of the female frog, Rana esculenta. Fluctuations throughout the reproductive cycle. Brain Res. 2000, 880:92-101.
143. Do Rego J.L., Seong J.Y., Burel D., Luu-The V., Larhammar D., Tsutsui K., Pelletier G., Tonon M.C., Vaudry H. Steroid biosynthesis within the frog brain: a model of neuroendocrine regulation. Ann. N. Y. Acad. Sci. 2009, 1163:83-92.
144. Mensah-Nyagan A.G., Do-Rego J.L., Beaujean D., Luu-The V., Pelletier G., Vaudry H. Regulation of neurosteroid biosynthesis in the frog diencephalon by GABA and endozepines. Horm. Behav. 2001, 40:218-225.
145. Vaudry H., Do Rego J.L., Burel D., Luu-The V., Pelletier G., Vaudry D., Tsutsui K. Neurosteroid biosynthesis in the brain of amphibians. Front. Endocrinol. 2011, 2:79.
146. Iwabuchi J., Wako S., Tanaka T., Ishikawa A., Yoshida Y., Miyata S. Analysis of the p450 aromatase gene expression in the Xenopus brain and gonad. J. Steroid Biochem. Mol. Biol. 2007, 107:149-155.
147. Kuntz S., Chesnel A., Flament S., Chardard D. Cerebral and gonadal aromatase expressions are differently affected during sex differentiation of Pleurodeles waltl. J. Mol. Endocrinol. 2004, 33:717-727.
148. Langlois V.S., Carew A.C., Pauli B.D., Wade M.G., Cooke G.M., Trudeau V.L. Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms. Environ. Health Perspect. 2010, 118:552-557.
149. Langlois V.S., Duarte-Guterman P., Trudeau V.L. Expression profiles of reproduction- and thyroid hormone-related transcripts in the brains of chemically-induced intersex frogs. Sex. Dev. 2011, 5:26-32.
150. Urbatzka R., Lutz I., Kloas W. Aromatase, steroid-5-alpha-reductase type 1 and type 2 mRNA expression in gonads and in brain of Xenopus laevis during ontogeny. Gen. Comp. Endocrinol. 2007, 153:280-288.
151. Kuntz S., Chardard D., Chesnel A., Ducatez M., Callier M., Flament S. Expression of aromatase and steroidogenic factor 1 in the lung of the urodele amphibian Pleurodeles waltl. Endocrinology 2004, 145:3111-3114.
152. Coumailleau P., Kah O. Cyp19a1 (aromatase) expression in the Xenopus brain at different developmental stages. J. Neuroendocrinol. 2014, 26:226-236.
153. Burrone L., Santillo A., Pinelli C., Baccari G.C., Di Fiore M.M. Induced synthesis of P450 aromatase and 17beta-estradiol by d-aspartate in frog brain. J. Exp. Biol. 2012, 215:3559-3565.
154. Nakagawa T., Iwabuchi J. Brain-specific promoter/exon I.f of the cyp19a1 (aromatase) gene in Xenopus laevis. J. Steroid Biochem. Mol. Biol. 2012, 132:247-255.
155. Miyata S., Kubo T. In vitro effects of estradiol and aromatase inhibitor treatment on sex differentiation in Xenopus laevis gonads. Gen. Comp. Endocrinol. 2000, 119:105-110.
156. Okada G., Maruo K., Funada S., Nakamura M. Differential display analysis of gene expression in female-to-male sex-reversing gonads of the frog Rana rugosa. Gen. Comp. Endocrinol. 2008, 155:623-634.
157. Villalpando I., Merchant-Larios H. Determination of the sensitive stages for gonadal sex-reversal in Xenopus laevis tadpoles. Int. J. Dev. Biol. 1990, 34:281-285.
158. Hayes T.B. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J. Exp. Zool. 1998, 281:373-399.
159. Mackenzie C.A., Berrill M., Metcalfe C., Pauli B.D. Gonadal differentiation in frogs exposed to estrogenic and antiestrogenic compounds. Environ. Toxicol. Chem. 2003, 22:2466-2475.
160. Kloas W. Amphibians as a model for the study of endocrine disruptors. Int. Rev. Cytol. 2002, 216:1-57.
161. Hogan N.S., Duarte P., Wade M.G., Lean D.R., Trudeau V.L. Estrogenic exposure affects metamorphosis and alters sex ratios in the northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. Gen. Comp. Endocrinol. 2008, 156:515-523.
162. Szymanski L., Bakker J. Aromatase knockout mice show normal steroid-induced activation of gonadotrophin-releasing hormone neurones and luteinising hormone surges with a reduced population of kisspeptin neurones in the rostral hypothalamus. J. Neuroendocrinol. 2012, 24:1222-1233.
163. Kloas W., Urbatzka R., Opitz R., Wurtz S., Behrends T., Hermelink B., Hofmann F., Jagnytsch O., Kroupova H., Lorenz C., Neumann N., Pietsch C., Trubiroha A., Van Ballegooy C., Wiedemann C., Lutz I. Endocrine disruption in aquatic vertebrates. Ann. N. Y. Acad. Sci. 2009, 1163:187-200.
164. Cevasco A., Urbatzka R., Bottero S., Massari A., Pedemonte F., Kloas W., Mandich A. Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: II. Effects on gonad histomorphology. Comp. Biochem. Physiol. Toxicol. Pharmacol. 2008, 147:241-251.
165. Tompsett A.R., Wiseman S., Higley E., Giesy J.P., Hecker M. Effects of exposure to 17alpha-ethynylestradiol during larval development on growth, sexual differentiation, and abundances of transcripts in the liver of the wood frog (Lithobates sylvaticus). Aquat. Toxicol. 2013, 126:42-51.
166. Duarte-Guterman P., Navarro-Martin L., Trudeau V.L. Mechanisms of crosstalk between endocrine systems: regulation of sex steroid hormone synthesis and action by thyroid hormones. Gen. Comp. Endocrinol. 2014, in press [Epub ahead of print].
167. 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.
168. Ijiri S., Berard C., Trant J.M. Characterization of gonadal and extra-gonadal forms of the cDNA encoding the Atlantic stingray (Dasyatis sabina) cytochrome P450 aromatase (CYP19). Mol. Cell. Endocrinol. 2000, 164:169-181.
169. Ijiri S., Kazeto Y., Lokman P.M., Adachi S., Yamauchi K. Characterization of a cDNA encoding P-450 aromatase (CYP19) from Japanese eel ovary and its expression in ovarian follicles during induced ovarian development. Gen. Comp. Endocrinol. 2003, 130:193-203.
170. Jeng S.R., Dufour S., Chang C.F. Differential expression of neural and gonadal aromatase enzymatic activities in relation to gonadal development in Japanese eel, Anguilla japonica. J. Exp. Zool. A Comp. Exp. Biol. 2005, 303:802-812.
171. Jeng S.R., Pasquier J., Yueh W.S., Chen G.R., Lee Y.H., Dufour S., Chang C.F. Differential regulation of the expression of cytochrome P450 aromatase, estrogen and androgen receptor subtypes in the brain-pituitary-ovarian axis of the Japanese eel (Anguilla japonica) reveals steroid dependent and independent mechanisms. Gen. Comp. Endocrinol. 2012, 175:163-172.
172. Henkel C.V., Burgerhout E., de Wijze D.L., Dirks R.P., Minegishi Y., Jansen H.J., Spaink H.P., Dufour S., Weltzien F.A., Tsukamoto K., van den Thillart G.E. Primitive duplicate Hox clusters in the European eel's genome. PLoS One 2012, 7:e32231.
173. Choi K.M., Kim J.Y., Kim Y. Distribution of the immunoreactivity for glycoprotein M6B in the neurogenic niche and reactive glia in the injury penumbra following traumatic brain injury in mice. Exp. Neurobiol. 2013, 22:277-282.
174. Goldshmit Y., Frisca F., Pinto A.R., Pebay A., Tang J.K., Siegel A.L., Kaslin J., Currie P.D. Fgf2 improves functional recovery-decreasing gliosis and increasing radial glia and neural progenitor cells after spinal cord injury. Brain Behav. 2014, 4:187-200.
175. Guo Y., Wei Q., Huang Y., Xia W., Zhou Y., Wang S. The effects of astrocytes on differentiation of neural stem cells are influenced by knock-down of the glutamate transporter, GLT-1. Neurochem. Int. 2013, 63:498-506.
176. Saha B., Peron S., Murray K., Jaber M., Gaillard A. Cortical lesion stimulates adult subventricular zone neural progenitor cell proliferation and migration to the site of injury. Stem Cell Res. 2013, 11:965-977.
177. Costa M.R., Gotz M., Berninger B. What determines neurogenic competence in glia?. Brain Res. Rev. 2010, 63:47-59.