Estrogen increases the number of spinophilin-immunoreactive spines in the hippocampus of young and aged female rhesus monkeys

Journal of Comparative Neurology

Volumn 465, Issue 4, 2003, Pages 540-550

  Hao, Jiandong ^a   Janssen, William G M ^a   Tang, Yong ^a   Roberts, Jeffrey A ^b   McKay, Heather ^b   Lasley, Bill ^b   Allen, Patrick B ^c   Greengard, Paul ^c   Rapp, Peter R ^a   Kordower, Jeffrey H ^d   Hof, Patrick R ^a   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Aging; Estrogen replacement therapy; Monkey hippocampus; Optical fractionator; Total spine number

Indexed keywords

ESTRADIOL CIPIONATE; ESTROGEN; PROTEIN; SPINOPHILIN; UNCLASSIFIED DRUG;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; ESTROGEN ACTIVITY; ESTROGEN THERAPY; FEMALE; HIPPOCAMPUS; IMMUNOLOCALIZATION; NONHUMAN; OVARIECTOMY; POSTMENOPAUSE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RHESUS MONKEY; STATISTICS; STEREOLOGY;

AGE FACTORS; ANIMALS; BIOLOGICAL MARKERS; COGNITION DISORDERS; DENDRITES; DENTATE GYRUS; DRUG ADMINISTRATION SCHEDULE; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; ESTROUS CYCLE; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MICROFILAMENT PROTEINS; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; OVARIECTOMY; POSTMENOPAUSE;

EID: 0037619881     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10837     Document Type: Article

References (63)

1. Adams MM, Shah RA, Janssen WGM, Morrison JH. 2001. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci USA 98:8071-8076.
2. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, Morrison JH. 2002. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 22:3608-3614.
3. Akama KT, McEwen BS. 2003. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 23:2333-2339.
4. Allen PB, Ouimet CC, Greengard P. 1997. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 94:9956-9961.
5. Bellino FL, Wise PM. 2003. Nonhuman primate models of menopause workshop. Biol Reprod 68:10-18.
6. Bimonte HA, Denenberg VH. 1999. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24:161-173.
7. Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, Greengard P, McEwen BS. 2001. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 142:1284-1289.
8. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
9. Chesler EJ, Juraska JM. 2000. Administration estrogen and progesterone impairs spatial reference memory in ovariectomized rats. Horm Behav 38:234-242.
10. Daniel JM, Roberts SL, Dohanich GP. 1999. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiol Behav 66:11-20.
11. Engert F, Bonhoeffer T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
12. Fader AJ, Hendricson AW, Dohanich GP. 1998. Estrogen improves performance of reinforced T-maze alteration and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol Learn Mem 69:225-240.
13. Fader AJ, Johnson PEM, Dohanich GP. 1999. Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine on a radial-arm maze. Pharmacol Biochem Behav 62:711-717.
14. Feng J, Yan Z, Ferreira A, Tomizawa K, Liauw JA, Zhuo M, Allen PB, Ouimet CC, Greengard P. 2000. Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci USA 97:9287-9292.
15. Folstein MF, Folstein SE, McHugh PR. 1975. "Mini-Mental State. " A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198.
16. Gallagher M, Rapp PR. 1997. The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339-370.
17. Gazzaley AH, Weiland NG, McEwen BS, Morrison JH. 1996. Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16:6830-6838.
18. Gazzaley A, Kay S, Benson DL. 2002. Dendritic spine plasticity in hippocampus. Neuroscience 111:853-862.
19. Geinisman Y, DeToledo-Morrell L, Morrell F. 1986. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc Natl Acad Sci USA 83:3027-3031.
20. Geinisman Y, DeToledo-Morrell L, Morrell F, Heller RE. 1995. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog Neurobiol 45:223-252.
21. Gibbs RB. 1999. Estrogen replacement enhances acquisition of apatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm Behav 36:222-233.
22. Gibbs RB. 2000. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 21:107-116.
23. Gibbs RB, Burke AM, Johnson DA. 1998. Estrogen replacement attenuates effects of scopolamine and Lorazepam on memory acquisition and retention. Horm Behav 34:112-125.
24. Gould E, Woolley CS, Frankfuit M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood J Neurosci 10:1286-1291.
25. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ. 1988. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96:379-394.
26. Hays J, Ockene JK, Brunner RL, Kotchen JM, Manson JE, Patterson RE, Aragaki AK, Shumaker SA, Brzyski RG, LaCroix AZ, Granek IA, Valanis BG. 2003. Effects of estrogen plus progestin on health-related quality of life. N Engl J Med 348:1839-1854.
27. Hjelle OP, Chaudhry FA, Ottersen OP. 1994. Antisera to glutathione: characterization and immunocytochemical application to the rat cerebellum. Eur J Neurosci 6:793-804.
28. Kampan DL, Sherwin BB. 1994. Estrogen use and verbal memory in Healthy postmenopausal women. Obstet Gynecol 83:979-983.
29. Kimura D. 1995. Estrogen replacement therapy may protect against intellectual decline in postmenopausal women. Horm Behav 29:312-321.
30. Korol DL, Manning CA. 2001. Effects of estrogen on cognition: implications for menopause. In: Carroll ME, Overmier JB (eds), Animal Research and Human Health: Advancing Human Welfare Through Behavioral Science. American Psychological Association Book Publishers, Washington D.C. p 305-322.
31. Lamberts SWJ, van den Beld AW, van der Lely AJ. 1997. The endocrinology of aging. Science 278:419-424.
32. Leranth C, Shanabrough M, Remond DE. 2002. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol 447:34-42.
33. Luine V, Richards ST, Wu VY, Beck KD. 1998. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34:149-162.
34. Maletic-Savatic M, Malinow R, Svoboda K. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
35. Markham JA, Pych JC, Juraska JM. 2002. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav 42:284-293.
36. McEwen B. 2002. Estrogen actions throughout the brain. Rec Prog Horm Res 57:357-84.
37. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagen L, Alves SE. 2001. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429:335-371.
38. Nimchinsky EA, Sabatini BL, Svoboda K. 2002. Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
39. O'Connell MB. 1995. Pharmacokinetic and pharmacologic variation between different estrogen products. J Clin Pharmacol 35:18S-24S.
40. Packard MG. 1998. Posttraining estrogen and memory modulation. Horm Behav 34:126-139.
41. Phillips SM, Sherwin BB. 1992. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 17:485-495.
42. Rapp PR, Morrison JH, Roberts JA. 2003. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci (in press).
43. Resnick SM, Henderson VW. 2002. Hormone therapy and risk of Alzheimer disease: a critical time. JAMA 288:2170-2172.
44. Resnick SM, Metter EJ, Zonderman AB. 1997. Estrogen replacement therapy and longitudinal decline in visual memory. A possible protective effect? Neurology 49:1491-1497.
45. Resnick SM, Maki PM, Golski S, Kraut MA, Zonderman AB. 1998. Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Horm Behav 34:171-182.
46. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J, Writing Group for the Women's Health Initiative Investigators. 2002. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288:321-333.
47. Sandstrom NJ, Williams CL. 2001. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384-393.
48. Schmitz C, Hof PR. 2000. Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 20:93-114.
49. Shideler SE, Gee N, Chen J, Lasley BL. 2001. Estrogen and progesterone metabolites and follicle-stimulating hormone in the aged macaque female. Biol Reprod 65:1718-1725.
50. Smith SS, Hsu FC, Li X, Frye CA, Faber DS, Markowitz RS. 2000. Oestrogen effects in olivo-cerebellar and hippocampal circuits. Novartis Found Symp 230:155-168.
51. Tang Y, Janssen WGM, Hao J, Roberts J, McKay H, Hof PR, Morrison JH. 2002. Effects of estrogen on dendritic spines in prefrontal cortex of young female rhesus monkeys. Soc Neurosci Abstr 368.13 [http:// www.sfn.org].
52. van Lookeren Campagne M, Oestreicher AB, van der Krift TP, Gispen WH, Verkleij AJ. 1991. Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J Histochem Cytochem 39:1267-1279.
53. Warren SG, Juraska JM. 1997. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 111:259-266.
54. West MJ, Slomianka L, Gundersen HJG. 1991. Unbiased stereological setimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
55. Wise PM, Dubal DB, Wilson ME, Rau SW. 2000. Estradiol is a neuroprotective factor in in vivo and in vitro models of brain injury. J Neurocytol 29:401-410.
56. Woolley CS. 1998. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140-148.
57. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
58. Woolley CS, McEwen BS. 1993. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306.
59. Woolley CS, McEwen BS. 1994. Estradiol regulates hippocampal dendritic spine density via and N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
60. Woolley CS, Gould E, Frankfuit M, McEwen BS. 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
61. Yaffe K, Sawaya G, Lieberburg I, Grady D. 1998. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. JAMA 279:688-695.
62. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC, Breitner JC, Cache County Memory Study Investigators. 2002. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County study. JAMA 288:2123-2129.
63. Znamensky V, Akama KT, McEwen BS, Milner TA. 2003. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites. J Neurosci 23:2340-2347.