Effects of two years of conjugated equine estrogens on cholinergic neurons in young and middle-aged ovariectomized monkeys

Brain Research

Volumn 1264, Issue , 2009, Pages 13-23

  Browne, Carole ^a   Tobin, Joseph R ^b   Voytko, Mary Lou ^b  

^a WAKE FOREST UNIVERSITY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Diagonal band; Medial septum; Nucleus basalis; Ovariectomy; Premarin; Stereology

Indexed keywords

CONJUGATED ESTROGEN;

ADOLESCENT; AGE DISTRIBUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CHOLINERGIC NERVE CELL; COGNITION; CONTROLLED STUDY; DRUG SELECTIVITY; ESTROGEN ACTIVITY; FEMALE; FOREBRAIN; HISTOPATHOLOGY; MEYNERT BASAL NUCLEUS; MONKEY; NONHUMAN; OVARIECTOMY; POSTMENOPAUSE; PRIORITY JOURNAL; TISSUE SPECIFICITY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BASAL NUCLEUS OF MEYNERT; CELL COUNT; CELL SIZE; DIAGONAL BAND OF BROCA; ESTRADIOL; ESTROGENS, CONJUGATED (USP); FEMALE; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; NEURONS; OVARIECTOMY; SEPTAL NUCLEI; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EQUIDAE; MACACA FASCICULARIS;

EID: 63249117884     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.01.014     Document Type: Article

References (77)

1. Adams M.R., Kaplan J.R., Manuck S.B., Kroritnik D.R., Parks J.S., Wolfe M.S., and Clarkson T.B. Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys: lack of an effect of added progesterone. Arteriosclerosis 10 (1990) 1051-1057
2. Ancelin M.L., and Ritchie K. Lifelong endocrine fluctuations and related cognitive disorders. Curr. Pharm. Des. 11 (2005) 4229-4252
3. Appt S.E., Clarkson T.B., Lees C.J., and Anthony M.S. Low dose estrogens inhibit coronary artery atherosclerosis in postmenopausal monkeys. Maturitas 55 (2006) 187-194
4. Brinton R.D., Tran J., Proffitt P., and Montoya M. 17 beta-Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res. 22 (1997) 1339-1351
5. Brinton R.D., Chen S., Montoya M., Hsieh D., and Minaya J. The estrogen replacement therapy of the Women's Health Initiative promotes the cellular mechanisms of memory and neuronal survival in neurons vulnerable to Alzheimer's disease. Maturitas 34 Suppl. 2 (2000) S35-52
6. Calhoun M.E., Mao Y., Roberts J.A., and Rapp P.R. Reduction in hippocampal cholinergic innervation is unrelated to recognition memory impairment in aged rhesus monkeys. J. Comp. Neurol. 475 (2004) 238-246
7. Castner S.A., Goldman-Rakic P.S., and Williams G.V. Animal models of working memory: insights for targeting cognitive dysfunction in schizophrenia. Psychopharmacology 174 (2004) 111-125
8. Celik O., Erdem G., Hascalik S., Karakas H.M., and Tamser M. Magnetic resonance spectroscopic comparison of the effects of resveratrol (3,4′,5-trihydroxy stilbene) to conjugated equine estrogen, tibolone and raloxifene on ovariectomized rat brains. Eur. J. Obstet. Gynecol. Reprod. Biol. 120 (2005) 73-79
9. Clarkson T.B., Anthony M.S., and Wagner J.D. A comparison of tibolone and conjugated equine estrogens effects on coronary artery atherosclerosis and bone density of postmenopausal monkeys. J. Clin. Endocrinol. Metab. 86 (2001) 5396-5404
10. Clarkson T.B., Anthony M.S., Mikkola T.S., and St. Clair R.W. Comparison of tibolone and conjugated equine estrogens effects on carotid artery atherosclerosis of postmenopausal monkeys. atherosclerosis of postmenopausal monkeys. Stroke 33 (2002) 2700-2703
11. Clarkson T.B., Anthony M.S., Cline J.M., Lees C.J., and Ederveen A.G. Multisystem evaluations of the long-term effects of tibolone on postmenopausal monkeys. Maturitas 48 Suppl 1 (2004) S24-9
12. Conner J.M., Darracq M.A., Roberts J., and Tuszynski M.H. Nontropic actions of neurotrophins: subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation. Proc. Natl. Acad. Sci. 98 (2001) 1941-1946
13. Daniel J.M., and Dohanich G.P. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J. Neurosci. 21 (2001) 6949-6956
14. Daniel J.M., Hulst J.L., and Lee C.D. Role of hippocampal M2 muscarinic receptors in the estrogen-induced enhancement of working memory. Neuroscientist 132 (2005) 57-64
15. Dohanich G.P., Fader A.J., and Javorsky D.J. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behav. Neurosci. 108 (1994) 988-992
16. Dutar P., Bassant M.-H., Senut M.-C., and Lamour Y. The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 75 (1995) 393-427
17. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., Hsia J., Margolis K.L., Hogan P.E., Wallace R., Dailey M., Freeman R., Hays J., and Women's Health Initiative Memory Study. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291 (2004) 2959-2968
18. Everett B.J., and Robbins T.W. Central cholinergic systems and cognition. Ann. Rev. Psych. 48 (1997) 649-684
19. Fader A.J., Hendricson A.W., and Dohanich G.P. Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol. Learn. Mem. 69 (1998) 225-240
20. Gibbs R.B. Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm. Behav. 36 (1999) 222-223
21. Gibbs R.B. Oestrogen and the cholinergic hypothesis: implications for oestrogen replacement therapy in postmenopausal women. Novartis Found. Symp. 230 (2000) 94-111
22. Gibbs R.B. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm. Behav. 42 (2002) 245-275
23. Gibbs R.B. Estradiol enhances DMP acquisition via a mechanism not mediated by turning strategy but which requires intact basal forebrain cholinergic projections. Horm. Behav. 52 (2007) 352-359
24. Gibbs R.B., Burke A.M., and Johnson D.A. Estrogen replacement attenuates effects of scopolamine and lorazepam on memory acquisition and retention. Horm. Behav. 34 (1998) 112-125
25. Gibbs R.B., Nelson D., Anthony M.S., and Clarkson T.B. Effects of long-term hormone replacement and of tibolone on choline acetyltransferase and acetylcholinesterase activities in the brains of ovariectomized, cynomologus monkeys. Neuroscientist 113 (2002) 907-914
26. Gibbs R.B., Edwards D., Lazar N., Nelson D., and Talameh J. Effects of long-term hormone treatment and of tibolone on monoamines and monoamine metabolites in the brains of ovariectomised, cynomologous monkeys. J. Neuroendocrinol. 18 (2006) 643-654
27. Gilardi K.V.K., Shideler S.E., Valverde C.R., Roberts J.A., and Lasley B.L. Characterization of the onset of menopause in the rhesus macaque. Biol. Reprod. 57 (1997) 335-340
28. Gilmor M.L., Nash N.R., Roghani A., Edwards R.H., Yi H., Hersch S.M., and Levey A.I. Expression of the putative vesicular acetylcholine transporter in rat brain and the localization in cholinergic synaptic vesicles. J. Neurosci. 16 (1996) 2179-2190
29. Goodman A.L., Descalzi C.D., Johnson D.K., and Hodgen G.D. Composite pattern of circulating LH, FSH, estradiol and progesterone during the menstrual cycle in cynomolgus monkeys. Proc. Soc. Exp. Biol. Med. 155 (1997) 479-481
30. Gresack J.E., and Frick K.M. Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol. Biochem. Behav. 84 (2006) 112-119
31. Gunderson H.J.G. The efficiency of systematic sampling in stereology and its prediction. J. Micrsocopy 147 (1987) 229-263
32. Hopfinger J.B., Woldorff M.G., Fletcher E.M., and Mangun G.R. Dissociating top-down attentional control from selective perception and action. Neuropsychologia 39 (2001) 1277-1291
33. Jayo M.J., Register T.C., and Carlson C.S. Effects on bone of oral hormone replacement therapy initiated two years after treatment in young adult monkeys. Bone 23 (1998) 361-366
34. Jensen E.B.V., and Gunderson H.J.G. The rotator. J. Microsocopy 170 (1993) 35-44
35. Jerome C.P., Carlson C.S., Register T.C., Bain F.T., Jayo M.J., Weaver D.S., and Adams M.R. Bone functional changes in intact, ovariectomized hormone supplanted adult cynomolgus monkeys (Macaca fasicularis) evaluated by serum markers and dynamic histomorphometry. J. Bone Miner. Res. 9 (1994) 527-540
36. Jewett D.A., and Dukelow W.R. Cyclicity and gestation length of Macaca fascicularis. Primates 13 (1972) 327-330
37. 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. Mol. Brain Res. 142 (2005) 107-114
38. Johnson R.L., and Kapsalis E. Ageing, infecundity, and reproductive senescence in free-ranging female rhesus monkeys. J. Reprod. Fertil. 105 (1995) 271-278
39. Kompoliti K., Chu Y., Polish A., Roberts J., McCay H., Mufson E.J., Leurgans S., Morrison J.H., and Kordower J.H. Effects of estrogen replacement therapy on basal forebrain neurons and cortical cholinergic innervation in young and aged rhesus monkeys. J. Comp. Neurol. 472 (2004) 193-207
40. Kritzer M.F., and Kohama S.G. Ovarian hormones differentially influence immunoreactivity for dopamine β-hydroxylase, choline acetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys. J. Comp. Neurol. 409 (1999) 438-451
41. Lacreuse A. Effects of ovarian hormones on cognitive function in nonhuman primates. Neuroscientist 138 (2006) 859-867
42. LeBlanc E.S., Janowsky J., Chan B.K., and Nelson H.D. Hormone replacement therapy and cognition: systematic review and meta-analysis. JAMA 285 (2001) 1489-1499
43. Lees C., Shen V., and Brommage R. Effects of lasofozifene on bone in surgically postmenopausal cynomolgus monkeys. Menopause: J. North Amer. Menopause Soc. 14 (2007) 97-105
44. Maki P.M. A systematic review of clinical trials of hormone therapy on cognitive function: effects of age at initiation and progestin use. Ann. N. Y. Acad. Sci. 1052 (2005) 182-197
45. Maki P., and Hogervorst E. The menopause and HRT. HRT and cognitive decline. Best Pract. Res. Clin. Endocrinol. Metab. 17 (2003) 105-122
46. Mesulam M.M., Mufson E.J., Levey A.I., and Wainer B.H. 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 (1983) 190-197
47. Olton D.S., Markowska A.L., Voytko M.L., Given B., Gorman L., and Wenk G.L. Basal forebrain cholinergic system: a functional analysis. Adv. Exp. Med. Biol. 295 (1991) 353-372
48. Parent M.B., and Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn. Mem. 11 (2004) 9-20
49. Peeyananjarassri K., and Baber R. Effects of low-dose hormone therapy on menopausal symptoms, bone mineral density, endometrium, and the cardiovascular system: a review of randomized clinical trials. Climacteric 8 (2005) 13-23
50. Rapp P.R., Morrison J.H., and Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J. Neurosci. 23 (2003) 5708-5714
51. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., Gass M.L., Stefanick M.L., Lane D.S., Hays J., Johnson K.C., Coker L.H., Dailey M., and Bowen D. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289 (2003) 2663-2672
52. Rhodin J.A., Thomas T.N., Clark L., Garces A., and Bryant M. In vivo cerebrovascular actions of amyloid beta-peptides and the protective effect of conjugated estrogens. J. Alzheimer's Dis. 5 (2003) 275-286
53. Rico B., and Cavada C. A population of cholinergic neurons is present in the macaque monkey thalamus. Eur. J. Neurosci. 10 (1998) 2346-2352
54. Rozenberg S., Fellemans C., Kroll M., and Vandromme J. The menopause in Europe. Int. J. Fertil. Womens Med. 45 (2000) 182-189
55. Schafer M.K., Weihe E., Erickson J.D., and Eiden L.E. Human and monkey cholinergic neurons visualized in paraffin-embedded tissues by immunoreactivity for VAChT, the vesicular acetylcholine transporter. J. Mol. Neurosci. 6 (1995) 225-235
56. Shamy J.L., Buckmaster C.A., Amaral D.G., Calhoun M.E., and Rapp P.R. Reactive plasticity in the dentate gyrus following bilateral entorhinal cortex lesions in cynomolgus monkeys. J. Comp. Neurol. 502 (2007) 192-201
57. Sherwin B.B. Estrogen and cognitive aging in women. Neuroscientist 138 (2006) 1021-1026
58. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones III B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., and Wactawski-Wende J. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289 (2003) 2651-2662
59. Shumaker S.A., Legault C., Kuller L., Rapp S.R., Thal L., Lane D.S., Fillit H., Stefanick M.L., Hendrix S.L., Lewis C.E., Masaki K., and Coker L.H. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291 (2004) 2947-2958
60. Smith D.E., Roberts J., Gage F.H., and Tuszynski M.H. Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy. Proc. Natl. Acad. Sci. 96 (1999) 10893-10898
61. Smith D.E., Rapp P.R., McKay H.M., Roberts J.A., and Tuscynski M.H. Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. J. Neurosci. 24 (2004) 4373-4381
62. Speroff L., and Van de Wiele R.L. Regulation of the human menstrual cycle. Am. J. Obstet. Gynecol. 109 (1971) 234-247
63. Stroessner-Johnson H.M., Rapp P.R., and Amaral D.G. Cholinergic cell loss and hypertrophy in the medial septal nucleus of the behaviorally characterized aged Rhesus monkey. J. Neurosci. 12 (1992) 1936-1944
64. The Women's Health Initiative Steering Committee. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 291 (2004) 1701-1712
65. Tinkler G.P., and Voytko M.L. Estrogen modulates cognitive and cholinergic processes in surgically menopausal monkeys. Prog. Neuro-psychopharmacol. Biol. Psychiatry 29 (2005) 423-431
66. Tinkler G.P., Tobin J.R., and Voytko M.L. Effects of two years of estrogen loss or replacement on nucleus basalis cholinergic neurons and cholinergic fibers to the dorsolateral prefrontal and inferior parietal cortex of monkeys. J. Comp. Neurol. 469 (2004) 507-521
67. Vaucher E., Reymond I., Najaffe R., Kar S., Quirion R., Miller M.M., and Franklin K.B. Estrogen effects on object memory and cholinergic receptors in young and old female mice. Neurobiol. Aging 23 (2002) 87-95
68. Voytko M.L. Estrogen and the cholinergic system modulate visuospatial attention in monkeys (Macaca fascicularis). Behav. Neurosci. 116 (2002) 187-197
69. Voytko M.L. Functional and neurobiological similarities of aging in monkeys and humans. Age 20 (1997) 29-44
70. Voytko M.L., and Tinkler G.P. Cognitive function and its neural mechanisms in nonhuman primate models of aging, Alzheimer's disease and menopause. In: Taffee M.A., and Weed M.R. (Eds). Nonhuman Primate Models of Neuropsychopathology, Frontiers of Bioscience Special Edition. Front. Biosci. 9 (2004) 1899-1914
71. Voytko M.L., Olton D.S., Richardson R.T., Gorman L.K., Tobin J.R., and Price D.L. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J. Neurosci. 14 (1994) 167-186
72. Voytko M.L., Sukhov R.R., Walker L.C., Breckler S.J., Price D.L., and Koliatsos V.E. Neuronal number and size are preserved in the nucleus basalis of aged rhesus monkeys. Dementia 6 (1995) 131-141
73. Weihe E., Tao-Cheng J.-H., Schafer M.K.-H., Erickson J.D., and Eiden L.E. Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc. Natl. Acad. Sci. 93 (1996) 3547-3552
74. West M.J. New stereological methods for counting neurons. Neurobiol. Aging 14 (1993) 275-285
75. Woolfe N.J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37 (1991) 475-524
76. Writing Group for the Women's Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288 (2002) 321-333
77. Zurkovsky L., Brown S.L., Boyd S.E., Fell J.A., and Korol D.L. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscientist 144 (2007) 26-37