Both estrogen receptor α and estrogen receptor β agonists enhance cell proliferation in the dentate gyrus of adult female rats

Neuroscience

Volumn 141, Issue 4, 2006, Pages 1793-1800

  Mazzucco, C A ^a   Lieblich, S E ^a   Bingham, B I ^b   Williamson, M A ^b   Viau, V ^b   Galea, L A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Life Sciences Institute   (Canada)

Author keywords

adult neurogenesis; estradiol; estrogen receptors; hippocampus

Indexed keywords

BROXURIDINE; CELL MARKER; CORTICOSTEROID; DIARYLPROPIONITRILE; ESTRADIOL; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HORMONE RECEPTOR STIMULATING AGENT; KI 67 ANTIGEN; LIGAND; MESSENGER RNA; PROPYLPYRAZOLE TRIOL; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; FEMALE; GRANULE CELL; HIPPOCAMPUS; MODULATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; STATISTICAL ANALYSIS; STEM CELL;

ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; DENTATE GYRUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KI-67 ANTIGEN; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDES; NITRILES; PROPIONATES; PYRAZOLES; RATS;

EID: 33747428388     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.032     Document Type: Article

References (54)

1. Azcoitia I., Sierra A., and Garcia-Segura L.M. Localization of estrogen receptor beta-immunoreactivity in astrocytes of the adult rat brain. Glia 26 (1999) 260-267
2. Banasr M., Hery M., Brezun J.M., and Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 14 (2001) 1417-1424
3. Barkhem T., Carlsson B., Nilsson Y., Enmark E., Gustafsson J., and Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 54 (1998) 105-112
4. Blurton-Jones M., Kuan P.N., and Tuszynski M.H. Anatomical evidence for transsynaptic influences of estrogen on brain-derived neurotrophic factor expression. J Comp Neurol 468 (2004) 347-360
5. Brannvall K., Korhonen L., and Lindholm D. Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation. Mol Cell Neurosci 21 (2002) 512-520
6. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435 (2001) 406-417
7. Cameron H.A., Woolley C.S., McEwen B.S., and Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56 (1993) 337-344
8. Cardona-Gomez G.P., Mendez P., DonCarlos L.L., Azcoitia I., and Garcia-Segura L.M. Interactions of estrogens and insulin-like growth factor-I in the brain. implications for neuroprotection. Brain Res Brain Res Rev 37 (2001) 320-334
9. Cheng G., Weihua Z., Warner M., and Gustafsson J.A. Estrogen receptors ER alpha and ER beta in proliferation in the rodent mammary gland. Proc Natl Acad Sci U S A 101 (2004) 3739-3746
10. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., and Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23 (1999) 247-256
11. Frasor J., Barnett D.H., Danes J.M., Hess R., Parlow A.F., and Katzenellenbogen B.S. Response-specific and ligand dose-dependent modulation of estrogen receptor (ER) alpha activity by ERbeta in the uterus. Endocrinology 144 (2003) 3159-3166
12. Gibbs R.B. Estrogen and nerve growth factor-related systems in brain. Effects on basal forebrain cholinergic neurons and implications for learning and memory processes and aging. Ann N Y Acad Sci 743 (1994) 165-196 discussion 197-199
13. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
14. Gould E., Beylin A., Tanapat P., Reeves A., and Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2 (1999) 260-265
15. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., and Vesterby A. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96 (1988) 379-394
16. Hall J.M., and McDonnell D.P. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140 (1999) 5566-5578
17. Isgor C., and Watson S.J. Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience 134 (2005) 847-856
18. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., and Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 98 (2001) 4710-4715
19. Jin M., Jin F., Zhang L., Chen Z., and Huang H. Two estrogen replacement therapies differentially regulate expression of estrogen receptors alpha and beta in the hippocampus and cortex of ovariectomized rat. Brain Res Mol Brain Res 142 (2005) 107-114
20. Kalita K., Szymczak S., and Kaczmarek L. Non-nuclear estrogen receptor beta and alpha in the hippocampus of male and female rats. Hippocampus 15 (2005) 404-412
21. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., and Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 93 (1996) 5925-5930
22. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain. anatomical evidence of distinct roles of each subtype. J Neurobiol 36 (1998) 357-378
23. Li X., Schwartz P.E., and Rissman E.F. Distribution of estrogen receptor-beta-like immunoreactivity in rat forebrain. Neuroendocrinology 66 (1997) 63-67
24. Lu B., and Chow A. Neurotrophins and hippocampal synaptic transmission and plasticity. J Neurosci Res 58 (1999) 76-87
25. McEwen B., Akama K., Alves S., Brake W.G., Bulloch K., Lee S., Li C., Yuen G., and Milner T.A. Tracking the estrogen receptor in neurons. implications for estrogen-induced synapse formation. Proc Natl Acad Sci U S A 98 (2001) 7093-7100
26. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., and Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands. structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 44 (2001) 4230-4251
27. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491 (2005) 81-95
28. Nagy A.I., Ormerod B.K., Mazzucco C.A., and Galea L.A.M. Estradiol-induced enhancement in cell proliferation is mediated through estrogen receptors in the dentate gyrus of adult female rats. Drug Dev Res 66 (2006) 142-149
29. Orikasa C., McEwen B.S., Hayashi H., Sakuma Y., and Hayashi S. Estrogen receptor alpha, but not beta, is expressed in the interneurons of the hippocampus in prepubertal rats. an in situ hybridization study. Brain Res Dev Brain Res 120 (2000) 245-254
30. Ormerod B.K., and 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 102 (2001) 369-379
31. Ormerod B.K., Lee T.T., and 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 55 (2003) 247-260
32. Perez-Martin M., Azcoitia I., Trejo J.L., Sierra A., and Garcia-Segura L.M. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur J Neurosci 18 (2003) 923-930
33. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21 (2001) 7153-7160
34. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
35. Shughrue P.J., and Merchenthaler I. Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience 99 (2000) 605-612
36. Shughrue P.J., and Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol 436 (2001) 64-81
37. Simmons D.M., Arriza J.L., and Swanson L.W. A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA probes. J Histotechnol 12 (1989) 169-181
38. Simpkins J.W., Green P.S., Gridley K.E., Singh M., de Fiebre N.C., and Rajakumar G. Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease. Am J Med 103 (1997) 19S-25S
39. Smith M.T., Pencea V., Wang Z., Luskin M.B., and Insel T.R. Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39 (2001) 11-21
40. Sohrabji F., Miranda R.C., and Toran-Allerand C.D. Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92 (1995) 11110-11114
41. Solum D.T., and Handa R.J. Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. J Neurosci 22 (2002) 2650-2659
42. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., Katzenellenbogen B.S., and Katzenellenbogen J.A. Pyrazole ligands. structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 43 (2000) 4934-4947
43. Su J.D., Qiu J., Zhong Y.P., Li X.Y., Wang J.W., and Chen Y.Z. Expression of estrogen receptor (ER)-alpha and -beta immunoreactivity in hippocampal cell cultures with special attention to GABAergic neurons. J Neurosci Res 65 (2001) 396-402
44. Tanapat P., Hastings N.B., and Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 481 (2005) 252-265
45. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19 (1999) 5792-5801
46. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., and Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 437 (2001) 496-504
47. Thoenen H. Neurotrophins and activity-dependent plasticity. Prog Brain Res 128 (2000) 183-191
48. Toran-Allerand C.D., Ellis L., and Pfenninger K.H. Estrogen and insulin synergism in neurite growth enhancement in vitro. mediation of steroid effects by interactions with growth factors?. Brain Res 469 (1988) 87-100
49. Toran-Allerand C.D. Estrogen and the brain. Beyond ER-α, ER-β, and 17β-Estradiol. Ann N Y Acad Sci 1052 (2005) 136-144
50. Toran-Allerand C.D., Guan X., MacLusky N.J., Horvath T.L., Diano S., Singh M., Connolly Jr. E.S., Nethrapalli I.S., and Tinnikov A.A. ER-X. a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 22 (2002) 8391-8401
51. Viau V., and Sawchenko P. Hypothalamic neurons of the paraventricular nucleus respond in spatially, temporally and phenotypically differentiated manners to acute vs. repeated restraint stress. J Comp Neurol 445 (2002) 293-307
52. Watts A.G., and Swanson L.W. Diurnal variations in the content of preprocorticotropin-releasing hormone messenger ribonucleic acids in the hypothalamic paraventricular nucleus of rats of both sexes as measured by in situ hybridization. Endocrinology 125 (1989) 1734-1738
53. Weiland N.G., Orikasa C., Hayashi S., and McEwen B.S. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 388 (1997) 603-612
54. Ziylan Y.Z., Lefauconnier J.M., Bernard G., and Bourre J.M. Blood-brain barrier permeability. regional alterations after acute and chronic administration of ethinyl estradiol. Neurosci Lett 118 (1990) 181-184