Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus

Journal of Comparative Neurology

Volumn 474, Issue 3, 2004, Pages 419-426

  Adams, Michelle M ^a   Fink, Susan E ^a   Janssen, William G M ^a   Shah, Ravi A ^a   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Electron microscopy; Excitatory amino acids; Glutamate receptor; Hormone replacement; Reproductive senescence; Synapse

Indexed keywords

ESTROGEN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; ENDOCRINE SYSTEM; ESTROGEN THERAPY; FEMALE; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

AGING; ANIMALS; ESTROGENS; FEMALE; HIPPOCAMPUS; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 2642562084     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20148     Document Type: Article

References (42)

1. Adams MM, Morrison JH. 2003. Estrogen and the aging hippocampal synapse. Cereb Cortex 13:1271-1275.
2. Adams MM, Morrison JH, Gore AC. 2001a. NMDA receptor subunit mRNA levels change during reproductive senescence in hippocampus of female rats. Exp Neurol 170:171-179.
3. Adams MM, Oung T, Morrison JH, Gore AC. 2001b. Length of post-ovariectomy interval and age, but not estrogen replacement, regulate N-methyl-D-aspartate receptor mRNA levels in the hippocampus of female rats. Exp Neurol 170:345-356.
4. Adams MM, Shah RA, Janssen WGM, Morrison JH. 2001c. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci U S A 98:8071-8076.
5. Adams MM, Fink SE, Shah RA, Janssen WGM, 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.
6. Barnes CA, Rao G, Houston FP. 2000. LTP induction threshold change in old rats at the perforant path-granule cell synapse. Neurobiol Aging 21:613-620.
7. Barnes CA, Suster MS, Shen J, McNaughton BL. 1997. Multistability of cognitive maps in the hippocampus of old rats. Nature 388:272-275.
8. Blackstad TW, Karagülle T, Ottersen OP. 1990. MORFOREL, a computer program for two-dimensional analysis of micrographs of biological specimens, with emphasis on immunogold preparations. Comput Biol Med 20:15-34.
9. 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.
10. Córdoba Montoya DA, Carrer HF. 1997. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430-438.
11. Finch CE, Felicio LS, Mobbs CV, Nelson JF. 1984. Ovarian and steroidal influences on neuroendocrine aging processes in female rodents. Endocr Rev 5:467-497.
12. Fink G. 1986. The endocrine control of ovulation. Sci Prog 70:403-423.
13. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW. 1999. 17 β-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81:925-929.
14. Funabashi T, Kleopoulos SP, Kimura F, Mobbs CV. 1998. Changes in neurotensin mRNA by estrogen in the female rat preoptic area during aging: an in situ hybridization histochemistry study. Gen Comp Endocrinol 112:364-371.
15. 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.
16. Geinisman Y, de Toledo-Morrell L, Morrell F, Persina IS, Rossi M. 1992. Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the denate gyrus of aged rats. Hippocampus 2:445-456.
17. Gould E, Woolley CS, Frankfurt M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 4:1286-1291.
18. Hjelle OP, Chaudhry FA, Ottersen OP. 1994. Antisera to glutathione: characterization and immunocytochemical application to the rat cerebellum. Eur J Neurosci 6:794-804.
19. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
20. Lauber AH, Romano GJ, Mobbs CV, Howells RD, Pfaff DW. 1990. Estradiol induction of proenkephalin messenger RNA in hypothalamus: dose-response and relation to reproductive behavior in the female rat. Brain Res. Mol Brain Res 8:47-54.
21. Lu JK, Anzalone CK, Lapolt PS. 1994. Relation of neuroendocrine function to reproductive decline during aging in the female rat. Neurobiol Aging 15:541-544.
22. Miranda P, Williams CL, Einstein G. 1999. Granule cells in aging rats are sexually dimorphic in their response to estradiol. J Neurosci 19:3316-3325.
23. Murphy DD, Segal M. 1996. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068.
24. 2+ transients in spines of Cal pyramidal neurons from hippocampal slices. J Neurophysiol 81:1404-1411.
25. Racca C, Stephenson FA, Streit P, Roberts JDB, Somogyi P. 2000. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512-2522.
26. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA. 1997. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7:549-558.
27. Rubin BS. 2000. Hypothalamic alterations and reproductive aging in female rats: evidence of altered LHRH neuronal function. Biol Reprod 63:968-976.
28. Ruud HK, Blackstad TW. 1999. PALIREL, a computer program for analyzing particle-to-membrane relations, with emphasis on electron micrographs of immunocytochemical preparations and gold labeled molecules. Comput Biomed Res 32:93-122.
29. Takumi Y, Ramírez-León V, Laake P, Rinvik E, Ottersen OP. 1999. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
30. Tang Y, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. 1999. Genetic enhancement of learning and memory in mice. Nature 401:63-69.
31. Tovar KR, Westbrook GL. 1999. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
32. Tovar KR, Westbrook GL. 2002. Mobile NMDA receptors at hippocampal synapses. Neuron 34:255-264.
33. Valtschanoff JG, Weinberg RJ. 2001. Laminar organization of the NMDA receptor complex within the postsynaptic density. J Neurosci 21:1211-1217.
34. 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.
35. Weiland NG. 1992. Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology 131:662-668.
36. Wise PM, Kashon ML, Krajnak KM, Rosewell KL, Cai A, Scarbrough K, Harney JP, McShane T, Lloyd J, Weiland NG. 1997. Aging of the female reproductive systems: a window into brain aging. Recent Prog Horm Res 52:279-305.
37. Woolley CS. 1998. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140-148.
38. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuations in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
39. 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.
40. Woolley CS, McEwen BS. 1994. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
41. Woolley CW, Gould E, Frankfurt M, McEwen BS. 1990. Naturally occurring fluctuations in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
42. Woolley CS, Wenzel HJ, Schwartzkroin PA. 1996. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 373:108-117.