Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus

Brain Research

Volumn 1121, Issue 1, 2006, Pages 46-58

  Herrick, Scott P ^a,b   Waters, Elizabeth M ^b   Drake, Carrie T ^a   McEwen, Bruce S ^b   Milner, Teresa A ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Electron microscopy; Granule cell; Hippocampus; Interneuron; Neurogenesis; Rat; Synapse

Indexed keywords

BIOLOGICAL MARKER; DOUBLECORTIN; ESTROGEN RECEPTOR BETA;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN MITOCHONDRION; BRAIN TISSUE; CHEMICAL LABELING; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; FEMALE; GLIA CELL; INTERNEURON; NERVE CELL MEMBRANE; NEWBORN; NONHUMAN; PERIKARYON; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; DENTATE GYRUS; ESTROGEN RECEPTOR BETA; ESTRUS; FEMALE; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDES; PROESTRUS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33750702540     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.08.084     Document Type: Article

References (71)

1. Abraham I.M., Todman M.G., Korach K.S., and Herbison A.E. Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 145 (2004) 3055-3061
2. Abrous D.N., Koehl M., and Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85 (2005) 523-569
3. Althaus H.H., and Richter-Landsberg C. Glial cells as targets and producers of neurotrophins. Int. Rev. Cytol. 197 (2000) 203-277
4. Alvarez-Buylla A., Seri B., and Doetsch F. Identification of neural stem cells in the adult vertebrate brain. Brain Res. Bull. 57 (2002) 751-758
5. Azcoitia I., Sierra A., and Garcia-Segura L.M. Localization of estrogen receptor b-immunoreactivity in astrocytes of the adult rat brain. Glia 26 (1999) 260-267
6. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32 (2002) 235-249
7. Blurton-Jones M., and Tuszynski M.H. Estrogen receptor-beta colocalizes extensively with parvalbumin-labeled inhibitory neurons in the cortex, amygdala, basal forebrain, and hippocampal formation of intact and ovariectomized adult rats. J. Comp. Neurol. 452 (2002) 276-287
8. Bodo C., and Rissman E.F. New roles for estrogen receptor beta in behavior and neuroendocrinology. Front (2006) 4-5
9. 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
10. Brookmeyer R., Gray S., and Kawas C. Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset. Am. J. Public Health 88 (1998) 1337-1342
11. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
12. Bruel-Jungerman E., Laroche S., and Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci. 21 (2005) 513-521
13. Cahill C.M., Morinville A., Lee M.C., Vincent J.P., Collier B., and Beaudet A. Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J. Neurosci. 21 (2001) 7598-7607
14. Cammarata P.R., Chu S., Moor A., Wang Z., Yang S.H., and Simpkins J.W. Subcellular distribution of native estrogen receptor alpha and beta subtypes in cultured human lens epithelial cells. Exp. Eye Res. 78 (2004) 861-871
15. Carswell H.V., Macrae I.M., Gallagher L., Harrop E., and Horsburgh K.J. Neuroprotection by a selective estrogen receptor beta agonist in a mouse model of global ischemia. Am. J. Physiol.: Heart Circ. Physiol. 287 (2004) H1501-H1504
16. Chan J., Aoki C., and Pickel V.M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods 33 (1990) 113-127
17. Chen J.Q., Yager J.D., and Russo J. Regulation of mitochondrial respiratory chain structure and function by estrogens/estrogen receptors and potential physiological/pathophysiological implications. Biochim. Biophys. Acta 1746 (2005) 1-17
18. Commons K.G., and Milner T.A. Ultrastructural heterogeneity of enkephalin-containing neurons in the rat hippocampal formation. J. Comp. Neurol. 358 (1995) 324-342
19. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005) 1-14
20. Dhandapani K.M., and Brann D.W. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 67 (2002) 1379-1385
21. Dhandapani K., and Brann D. Neuroprotective effects of estrogen and tamoxifen in vitro: a facilitative role for glia?. Endocrine 21 (2003) 59-66
22. Dluzen D., and Horstink M. Estrogen as neuroprotectant of nigrostriatal dopaminergic system: laboratory and clinical studies. Endocrine 21 (2003) 67-75
23. Drake C.T., and Milner T.A. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res. 849 (1999) 203-215
24. Drake C.T., Milner T.A., and Patterson S.L. Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity. J. Neurosci. 19 (1999) 8009-8026
25. Eisch A.J. Adult neurogenesis: implications for psychiatry. In: Hofman M.A., Boer G.J., Holtmaat A.J.G.D., Van Someren E.J.W., Verhagen J., and Swaab D.F. (Eds). Prog. Brain Res. vol. 138 (2002), Elsevier Science 317-344
26. Eisch A.J., Barrot M., Schad C.A., Self D.W., and Nestler E.J. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7579-7584
27. Felty Q., and Roy D. Mitochondrial signals to nucleus regulate estrogen-induced cell growth. Med. Hypotheses 64 (2005) 133-141
28. Gould E., Tanapat P., Rydel T., and Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol. Psychiatry 48 (2000) 715-720
29. Herrick S.P., Waters E.M., McEwen B.S., Drake C.T., Alves S.E., and Milner T.A. Newly generated cells in dentate gyrus contain extranuclear estrogen receptor beta immunoreactivity. Abstr.-Soc. Neurosci. (2005) 403.7
30. Hrabovszky E., Kallo I., Steinhauser A., Merchenthaler I., Coen C.W., Petersen S.L., and Liposits Z. Estrogen receptor-beta in oxytocin and vasopressin neurons of the rat and human hypothalamus: immunocytochemical and in situ hybridization studies. J. Comp. Neurol. 473 (2004) 315-333
31. 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
32. Jessberger S., Romer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196 (2005) 342-351
33. Karten Y.J., Jones M.A., Jeurling S.I., and Cameron H.A. GABAergic signaling in young granule cells in the adult rat and mouse dentate gyrus. Hippocampus 16 (2006) 312-320
34. Koizumi H., Tanaka T., and Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49 (2006) 55-66
35. Leuner B., Mendolia-Loffredo S., Kozorovitskiy Y., Samburg D., Gould E., and Shors T.J. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J. Neurosci. 24 (2004) 7477-7481
36. Levin E.R. Cell localization, physiology, and nongenomic actions of estrogen receptors. J. Appl. Physiol. 91 (2001) 1860-1867
37. Liu S., Wang J., Zhu D.Y., Fu Y., Lukowiak K., and Lu Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J. Neurosci. 23 (2003) 732-736
38. Lobaton C.D., Vay L., Hernandez-Sanmiguel E., Santodomingo J., Moreno A., Montero M., and Alvarez J. Modulation of mitochondrial Ca(2+) uptake by estrogen receptor agonists and antagonists. Br. J. Pharmacol. 145 (2005) 862-871
39. Loy R., Gerlach J.L., and McEwen B.S. Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Dev. Brain Res. 39 (1989) 245-251
40. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., and 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)
41. McCarthy J.B., Barker-Gibb A.L., Alves S.E., and Milner T.A. TrkA immunoreactive astrocytes in dendritic fields of the hippocampal formation across estrous. Glia 38 (2002) 36-44
42. McEwen B.S. Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J. Appl. Physiol. 91 (2001) 2785-2801
43. 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
44. Mironov S.L., Ivannikov M.V., and Johansson M. [Ca2+]i Signaling between mitochondria and endoplasmic reticulum in neurons is regulated by microtubules: from mitochondrial permeability transition pore to Ca2+-induced Ca2+ release. J. Biol. Chem. 280 (2005) 715-721
45. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., Pfaff D.W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S., and Alves S.E. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144 (2003) 2055-2067
46. Moores C.A., Perderiset M., Francis F., Chelly J., Houdusse A., and Milligan R.A. Mechanism of microtubule stabilization by doublecortin. Mol. Cell 14 (2004) 833-839
47. Peters A., Palay S.L., and Webster H.D. The Fine Structure of the Nervous System. 3rd ed. (1991), Oxford Univ. Press, New York
48. Price Jr. R.H., Lorenzon N., and Handa R.J. Differential expression of estrogen receptor beta splice variants in rat brain: identification and characterization of a novel variant missing exon 4. Mol. Brain Res. 80 (2000) 260-268
49. Psarra A.M., Solakidi S., and Sekeris C.E. The mitochondrion as a primary site of action of steroid and thyroid hormones: presence and action of steroid and thyroid hormone receptors in mitochondria of animal cells. Mol. Cell. Endocrinol. 246 (2006) 21-33
50. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 19 (2004) 234-246
51. Saravia F., Revsin Y., Lux-Lantos V., Beauquis J., Homo-Delarche F., and De Nicola A.F. Oestradiol restores cell proliferation in dentate gyrus and subventricular zone of streptozotocin-diabetic mice. J. Neuroendocrinol. 16 (2004) 704-710
52. Scharfman H.E., Mercurio T.C., Goodman J.H., Wilson M.A., and MacLusky N.J. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J. Neurosci. 23 (2003) 11641-11652
53. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., and Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005) 348-356
54. 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
55. Shughrue P.J., and Merchenthaler I. Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience 99 (2000) 605-612
56. 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
57. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-a and -b mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997) 507-525
58. Simpkins J.W., Wang J., Wang X., Perez E., Prokai L., and Dykens J.A. Mitochondria play a central role in estrogen-induced neuroprotection. Curr. Drug Targets. CNS Neurol. Disord. 4 (2005) 69-83
59. Singer C.A., Figueroa-Masot X.A., Batchelor R.H., and Dorsa D.M. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19 (1999) 2455-2463
60. Snyder J.S., Hong N.S., McDonald R.J., and Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130 (2005) 843-852
61. Solum D.T., and Handa R.J. Localization of estrogen receptor alpha (ER alpha) in pyramidal neurons of the developing rat hippocampus. Brain Res. Dev. Brain Res. 128 (2001) 165-175
62. 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
63. 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
64. Thomas G.M., and Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev., Neurosci. 5 (2004) 173-183
65. Turner C.D., and Bagnara J.T. General Endocrinology (1971), W.B. Saunders, Philadelphia
66. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., and Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 19 (1999) 10372-10382
67. Wadiche L.O., Bromberg D.A., Bensen A.L., and Westbrook G.L. GABAergic signaling to newborn neurons in dentate gyrus. J. Neurophysiol. 94 (2005) 4528-4532
68. 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
69. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., and Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006) 296-304
70. Woolley C.S. Effects of estrogen in the CNS. Curr. Opin. Neurobiol. 9 (1999) 349-354
71. Yang S.H., Liu R., Perez E.J., Wen Y., Stevens Jr. S.M., Valencia T., Brun-Zinkernagel A.M., Prokai L., Will Y., Dykens J., Koulen P., and Simpkins J.W. Mitochondrial localization of estrogen receptor beta. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 4130-4135