Estrogen receptor immunoreactivity in the adult primate brain: Neuronal distribution and association with p75, trkA, and choline acetyltransferase

Journal of Comparative Neurology

Volumn 405, Issue 4, 1999, Pages 529-542

  Blurton Jones, M M ^a   Roberts, J A ^b   Tuszynski, M H ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Alzheimer's disease; Amygdala; Hippocampus; Nerve growth factor; Neurotrophins; Septal nucleus

Indexed keywords

CHOLINE ACETYLTRANSFERASE; ESTROGEN RECEPTOR;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; FEMALE; HIPPOCAMPUS; HORMONE RECEPTOR INTERACTION; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; RHESUS MONKEY; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; CHOLINE O-ACETYLTRANSFERASE; FEMALE; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MALE; NEURONS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTORS, ESTROGEN; RECEPTORS, NERVE GROWTH FACTOR; TISSUE DISTRIBUTION;

EID: 0033594230     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990322)405:4<529::AID-CNE6>3.0.CO;2-Y     Document Type: Article

References (84)

1. Bartus RT, Dean RL, Beer B, Lippa AS. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-417.
2. Behl C, Widmann M, Trapp T, Holsboer F. 1995. 17-beta-Estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun 216:473-482.
3. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F. 1997. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
4. Bevitt DJ, Milton ID, Piggot N, Henry L, Carter MJ, Toms GL, Lennard TW, Westley B, Angus B, Home CH. 1997. New monoclonal antibodies to oestrogen and progsterone receptors effective for paraffin section immunohistochemistry. J Pathol 183:228-232.
5. Blaustein JD, Turcotte JC. 1989. Estrogen receptor-immunostaining of neuronal cytoplasmic processes as well as cell nuclei in guinea pig brain. Brain Res 495:75-82.
6. Blaustein JD. 1992. Cytoplasmic estrogen receptors in rat brain: immunocytochemical evidence using three antibodies with distinct epitopes. Endocrinology 131:1336-1342.
7. Blaustein JD, Lehman MN, Turcotte JC, Greene G. 1992. Estrogen receptors in dendrites and axon terminals in the guinea pig hypothalamus. Endocrinology 131:281-290.
8. Borhegyi Z, Magloczky Z, Acsady L, Freund TF. 1998. The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex. Neuroscience 82:1053-1065.
9. Buzsaki G. 1984. Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131-153.
10. Chen EY, Mufson EJ, Kordower JH. 1996. TRK and p75 neurotrophin receptor systems in the developing human brain. J Comp Neurol 369:591-618.
11. Conner JM, Varon S. 1992. Distribution of nerve growth factor-like immunoreactive neurons in the adult rat brain following colchicine treatment. J Comp Neurol 326:347-362.
12. Conner JL, Lauterborn JC, Van Q, Gall CM, Varon S. 1997. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17:2295-2313.
13. Coyle JT, Price PH, Delong MR. 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219:1184-1189.
14. Davies P, Maloney AJF. 1976. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2:1403.
15. DonCarlos LL, Monroy E, Morrell JI. 1991. Distribution of estrogen receptor-immunoreactive cells in the forebrain of the female guinea pig. J Comp Neurol 305:591-612.
16. Emerich DW, Winn S, Harper J, Hammang JP, Baetge EE, Kordower JH. 1994. Implants of polymer-encapsulated human NGF-secreting cells in the nonhuman primate: rescue and sprouting of degenerating cholinergic basal forebrain neurons. J Comp Neurol 349:148-164.
17. Emre M, Heckers S, Mash DC, Geula C, Mesulam MM. 1993. Cholinergic innervation of the amygdaloid complex in the human brain and its alterations in old age and Alzheimer's disease. J Comp Neurol 336:117-134.
18. Emson PC, Paxinos G, Le Gal La Salle G, Ben-Ari Y, Silver A. 1979. Choline acetyltransferase and acetylcholinesterase containing projections from the basal forebrain to the amygdaloid complex of the rat. Brain Res 165:271-282.
19. Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH. 1987. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329:65-68.
20. Gibbs RB, Pfaff DW. 1992. Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116:23-39.
21. Gibbs RB, Wu D, Hersh LB, Pfaff DW. 1994. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol 129:70-80.
22. Gibbs RB. 1996. Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res 720:61-68.
23. Gibbs RB. 1998a. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp Neurol 151:289-302.
24. Gibbs RB. 1998b. Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res 787:259-268.
25. Haglund L, Swanson LW, Kohler C. 1984. The projection of the supramam-millary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat. J Comp Neurol 229:171-185.
26. Heckers S, Geula C, Mesulam MM. 1992. Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325:68-82.
27. Heckers S, Mesulam MM. 1994. Two types of cholinergic projections to the rat amygdala. Neuroscience 60:383-397.
28. Hefti F. 1986. Nerve growth factor promotes survival of septal cholinergic neurons after injury. In: Fisher A, Hanin I, Lachman C, editors. Alzheimer's and Parkinson's disease: strategies for research and development. New York: Plenum, pp 615-625.
29. Hempstead BL, Martin-Zanca D, Kaplan DR, Parada LF, Chao MV. 1991. High affinity NGF binding requires coexpression of the trk protooncogene and the low-affinity NGF receptor. Nature 350:678-682.
30. Honjo H, Tanaka K, Kashiwagi T, Urabe M, Okada H, Hayashi M, Hayashi K. 1995. Senile dementia-Alzheimer's type and estrogen. Horm Metab Res 27:204-207.
31. Huerta PT, Lisman JE. 1993. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.
32. Ichikawa T, Shimizu T. 1998. Organization of choline acetyltransferase-containing structures in the cranial nerve motor nuclei and spinal cord of the monkey. Brain Res 779:96-103.
33. Jaffe AB, Toran-Allerand CD, Greengard P, Gandy SE. 1994. Estrogen regulates metabolism of Alzheimer amyloid beta precursor protein. J Biol Chem 269:13065-13068.
34. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF. 1991. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252:554-560.
35. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A, Bacal C, Lingle DD, Metter E. 1997. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. Neurology 48:1517-1521.
36. Keefer DA, Stumpf WE. 1975. Atlas of estrogen-concentrating cells in the central nervous system of the squirrel monkey. J Comp Neurol 160:419-441.
37. Kimura H, Tago H, Akiyama H, Hersh LB, Tooyama I, McGeer PL. 1990. Choline acetyltransferase immunopositive neurons in the lateral septum. Brain Res 533:165-170.
38. Kirk IJ, McNaughton N. 1991. Supramammillary cell firing and hippocampal rhythmical slow activity. NeuroReport 2:723-725.
39. Kocsis B, Vertes RP. 1994. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14:7040-7052.
40. Kocsis B, Vertes RP. 1997. Phase relations of rhythmic neuronal firing in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane anesthetized rats. Hippocampus 7:204-214.
41. Koliatsos VE, Nauta HJ, Clatterbuck RE, Holtzman DM, Mobley WC, Price DL. 1990. Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in the monkey. J Neurosci 10:3801-3813.
42. Kordower JH, Bartus RT, Bothwell M, Schatteman G, Gash DM. 1988. Nerve growth factor receptor immunoreactivity in the nonhuman primate (Cebus apella): distribution, morphology, and colocalization with cholinergic enzymes. J Comp Neurol 277:465-186.
43. Kordower JH, Winn SR, Liu YT, Mufson EJ, Sladek JR, Hammang JP, Baetge EE, Emerich DF. 1994a. The aged monkey basal forebrain: rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc Natl Acad Sci 91:10898-10902.
44. Kordower JH, Chen EY, Sladek JRJ, Mufson EJ. 1994b. trk-immunoreactivity in the monkey central nervous system: forebrain. J Comp Neurol 349:20-35.
45. Lehman MN, Ebling FJ, Moenter SM, Karsch FJ. 1993. Distribution of estrogen receptor-immunoreactive cells in the sheep brain. Endocrinology 133:878-886.
46. Lewis Carl SA, Gillete-Ferguson I, Ferguson DG. 1993. An indirect immunofluorescence procedure for staining the same cryosection with two mouse monoclonal primary antibodies. J Histochem Cytochem 41:1273-1278.
47. Martin RF, Bowden DM. 1996. A stereotaxic template atlas of the macaque brain for digital imaging and quantitative neuroanatomy. Neuroimage 4:119-150.
48. McMillan PJ, Singer CA, Dorsa DM. 1996. The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J Neurosci 16:1860-1865.
49. Merari A, Ginton A. 1975. Characteristics of exaggerated sexual behavior induced by electrical stimulation of the medial preoptic area in male rats. Brain Res 86:97-108.
50. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. 1983. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170-197.
51. Miranda RC, Sohrabji F, Toran-Allerand CD. 1993. Estrogen target neurons co-localize the mRNAs for the neurotrophins and their receptors during development: a basis for the interactions of estrogen and the neurotrophins. Mol Cell Neurosci 4:510-525.
52. Mook-Jung I, Joo I, Sohn S, Kwon HJ, Huh K, Jung MW. 1997. Estrogen blocks neurotoxic effects of beta-amyloid (1-42) and induces neurite extension on B103 cells. Neurosci Lett 235:101-104.
53. Morse JK, Wiegand SJ, Anderson K, Cai N, Carnahan J, Miller J, DiStefano PS, Altar CA, Lindsay RM. 1993. Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J Neurosci 13:4146-4156.
54. Mufson EJ, Bothwell M, Hersh LB, Kordower JH. 1989. Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J Comp Neurol 285:196-217.
55. Mufson EJ, Conner JM, Varon S, Kordower JH. 1994. Nerve growth factor-like immunoreactive profiles in the primate basal forebrain and hippocampal formation. J Comp Neurol 341:507-519.
56. Pan WX, McNaughton N. 1997. The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764:101-108.
57. Parada LF, Tsoulfas P, Tessarollo L, Blair J, Reid SW, Soppet D. 1992. The Trk family of tyrosine kinases: receptors for NGF-related neurotrophins. Cold Spring Harbor Symp Quant Biol 57:43-51.
58. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387.
59. Pfaff D, Keiner M. 1973. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151:121-158.
60. Pfaff DW, Gerlach JL, McEwen BS, Ferin M, Carmel P, Zimmerman EA. 1976. Autoradiographic localization of hormone-concentrating cells in the brain of the female rhesus monkey. J Comp Neurol 170:279-293.
61. Ridley RM, Samson NA, Baker HF, Johnson JA. 1988. Visuospatial learning impairment following lesion of the cholinergic projection to the hippocampus. Brain Res 456:71-87.
62. Ridley RM, Aitken DM, Baker HF. 1989. Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus. Brain Res 502:306-318.
63. Ross AH, Grob P, Bothwell M. 1984. Characterization of nerve growth factor receptor in neural cest tumors using monoclonal antibodies. Proc Natl Acad Sci 81:6681-6685.
64. Schneider LS, Farlow MR, Henderson VW, Pogoda JM. 1996. Effects of estrogen replacement therapy on response to tacrine in patients with Alzheimer's disease. Neurology 46:1580-1584.
65. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388:507-525.
66. Snider RS, Lee JC. 1961. A stereotaxic atlas of the monkey brain (Macaca mulatta). Chicago: University of Chicago Press.
67. Sohrabji F, Miranda RC, Toran-Allerand CD. 1994a. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14:459-471.
68. Sohrabji F, Greene LA, Miranda RC, Toran-Allerand CD. 1994b. Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J Neurobiol 25:974-988.
69. Sohrabji F, Miranda RC, Toran-Allerand CD. 1995. Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:11110-11114.
70. Srivastava RA, Bhasin N, Srivastava N. 1996. Apolipoprotein E gene expression in various tissues of mouse and regulation by estrogen. Biochem Mol Biol Int 38:91-101.
71. Staubli U, Lynch G. 1987. Stable hippocampal long-term potentiation elicited by "theta" pattern stimulation. Brain Res 435:227-234.
72. Swanson LW, Kohler C, Bjorklund A. 1987. The limbic region I. The septohippocampal system. In: Bjorklund A, Hokfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy, Vol. 5: Integrated systems of the CNS, Part I. Hypothalamus, hippocampus, amygdala, retina. Amsterdam: Elsevier. pp 125-278.
73. Tago H, McGeer PL, Bruce G, Hersh LB. 1987. Distribution of choline acetyltransferase-containing neurons of the hypothalamus. Brain Res 415:49-62.
74. Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB. 1989. Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 495:271-297.
75. Tang MX, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R. 1996. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease [see comments]. Lancet 348:429-432.
76. Toran-Allerand CD, Miranda RC, Bentham WD, Sohrabji F, Brown TJ, Hochberg RB, MacLusky NJ. 1992. Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA 89:4668-4672.
77. Toran-Allerand CD. 1996. Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? J Steroid Biochem Mol Biol 56:169-178.
78. Tuszynski MH, U HS, Amaral DG, Gage FH. 1990. Nerve growth factor infusion in primate brain reduces lesion-induced cholinergic neuronal degeneration. J Neurosci 10:3604-3614.
79. Tuszynski MH, U HS, Gage FH. 1991. Recombinant human nerve growth factor infusions prevent cholinergic neuronal degeneration in the adult primate brain. Ann Neurol 30:625-636.
80. Vertes RP. 1992. PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neurol 326:595-622.
81. Vertes RP, Kocsis B. 1997. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
82. Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL. 1994. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14:167-186.
83. Whitehouse PJ, Price DJ, Clark A, Coyle JT, DeLong M. 1981. Alzheimer's disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 10:122-126.
84. Whitehouse PJ, Price DL, Struble RG, Clar AW, Coyle JT, Delong MR. 1982. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215:1237-1239.