Home LiteratureArticle Details
PMID: 11687663 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway.

Bi R, Foy MR, Vouimba RM, Thompson RF, Baudry M

Abstract

Hippocampal synaptic structure and function exhibit marked variations during the estrus cycle of female rats. Estradiol activates the mitogen-activated protein (MAP) kinase pathway in numerous cell types, and MAP kinase has been shown to play a critical role in the mechanisms underlying synaptic plasticity. Here, we report that endogenous estrogen produces a tonic phosphorylation/activation of extracellular signal-regulated kinase 2 (ERK2)/MAP kinase throughout the female rat brain and an increase in tyrosine phosphorylation of NR2 subunits of N-methyl-D-aspartate (NMDA) receptors. Moreover, cyclic changes in estrogen levels during the estrus cycle of female rats are associated with corresponding changes in the levels of activation of ERK2, the state of tyrosine phosphorylation of NR2 subunits of NMDA receptors, and the magnitude of long-term potentiation in hippocampus. Thus, cyclic changes in female sexual hormones result in marked variations in the state of activation of a major cellular signaling pathway critical for learning and memory and in a cellular model of learning and memory.

MeSH Terms
Animals Estradiol/physiology Estrus Female Hippocampus/enzymology,physiology MAP Kinase Signaling System Neuronal Plasticity Phosphorylation Rats Rats, Sprague-Dawley Synapses/physiology
Chemicals
Estradiol
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bi R
Neuroscience Program, University of Southern California, Los Angeles, CA 90089-2520, USA.
Foy M R
Vouimba R M
Thompson R F
Baudry M
References (41)
41 references, click to expand
  1. The modulation of Pavlovian memory.
    Behav Brain Res. 2000 Jun 1;110(1-2):39-52 PMID: 10802302
  2. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus.
    Horm Behav. 1998 Oct;34(2):140-8 PMID: 9799624
  3. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters.
    Horm Behav. 1998 Oct;34(2):149-62 PMID: 9799625
  4. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat.
    J Neurosci. 1998 Dec 1;18(23):10037-44 PMID: 9822758
  5. P42/44 MAP kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro.
    J Neurophysiol. 1999 Jan;81(1):103-10 PMID: 9914271
  6. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation.
    J Neurophysiol. 1999 Feb;81(2):925-9 PMID: 10036289
  7. A necessity for MAP kinase activation in mammalian spatial learning.
    Learn Mem. 1999 Sep-Oct;6(5):478-90 PMID: 10541468
  8. Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region.
    Eur J Neurosci. 1999 Dec;11(12):4476-80 PMID: 10594677
  9. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-alpha knock-out mice.
    J Neurosci. 2000 Mar 1;20(5):1694-700 PMID: 10684871
  10. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3602-7 PMID: 10725383
  11. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons.
    J Neurosci. 1999 Apr 1;19(7):2455-63 PMID: 10087060
  12. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory.
    J Neurosci. 1999 May 1;19(9):3535-44 PMID: 10212313
  13. Novel mechanisms of estrogen action in the brain: new players in an old story.
    Front Neuroendocrinol. 1999 Apr;20(2):97-121 PMID: 10328986
  14. Src, a molecular switch governing gain control of synaptic transmission mediated by N-methyl-D-aspartate receptors.
    Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7697-704 PMID: 10393883
  15. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat.
    J Neurosci. 1999 Jul 15;19(14):5792-801 PMID: 10407020
  16. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning.
    J Neurosci. 2000 Nov 1;20(21):8177-87 PMID: 11050141
  17. A beneficial effect of estrogen on working memory in postmenopausal women taking hormone replacement therapy.
    Horm Behav. 2000 Dec;38(4):262-76 PMID: 11104644
  18. Estrogens: trophic and protective factors in the adult brain.
    Front Neuroendocrinol. 2001 Jan;22(1):33-66 PMID: 11141318
  19. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory.
    J Neurochem. 2001 Jan;76(1):1-10 PMID: 11145972
  20. Ras-related and MAPK signalling in neuronal plasticity and memory formation.
    Cell Mol Life Sci. 2000 Apr;57(4):604-11 PMID: 11130460
  21. Spatial reference memory and neocortical neurochemistry vary with the estrous cycle in C57BL/6 mice.
    Behav Neurosci. 2001 Feb;115(1):229-37 PMID: 11256446
  22. Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications.
    Annu Rev Pharmacol Toxicol. 2001;41:569-91 PMID: 11264469
  23. Memory retention is modulated by acute estradiol and progesterone replacement.
    Behav Neurosci. 2001 Apr;115(2):384-93 PMID: 11345963
  24. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: recent insights and remaining challenges.
    Learn Mem. 2001 May-Jun;8(3):121-33 PMID: 11390632
  25. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7093-100 PMID: 11416193
  26. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  27. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  28. Variations in memory function and sex steroid hormones across the menstrual cycle.
    Psychoneuroendocrinology. 1992 Oct;17(5):497-506 PMID: 1484916
  29. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism.
    J Neurosci. 1994 Dec;14(12):7680-7 PMID: 7996203
  30. How MAP kinases are regulated.
    J Biol Chem. 1995 Jun 23;270(25):14843-6 PMID: 7797459
  31. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase.
    Science. 1995 Dec 1;270(5241):1491-4 PMID: 7491495
  32. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats.
    Brain Res. 1995 Dec 12;703(1-2):26-30 PMID: 8719612
  33. NMDA channel regulation by channel-associated protein tyrosine kinase Src.
    Science. 1997 Jan 31;275(5300):674-8 PMID: 9005855
  34. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density.
    J Neurosci. 1997 Mar 1;17(5):1848-59 PMID: 9030643
  35. Spatial and nonspatial learning across the rat estrous cycle.
    Behav Neurosci. 1997 Apr;111(2):259-66 PMID: 9106666
  36. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task.
    Behav Neurosci. 1997 Apr;111(2):267-74 PMID: 9106667
  37. A role for the Ras signalling pathway in synaptic transmission and long-term memory.
    Nature. 1997 Nov 20;390(6657):281-6 PMID: 9384379
  38. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats.
    Brain Res. 1997 Dec 19;778(2):430-8 PMID: 9459564
  39. Novel mechanism for non-genomic action of 17 beta-oestradiol on kainate-induced currents in isolated rat CA1 hippocampal neurones.
    J Physiol. 1998 Feb 1;506 ( Pt 3):745-54 PMID: 9503335
  40. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons.
    J Neurosci. 1998 Apr 1;18(7):2550-9 PMID: 9502814
  41. Oestrogen and cognitive function throughout the female lifespan.
    Novartis Found Symp. 2000;230:188-96; discussion 196-201 PMID: 10965509
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-11-06
Epub
2001-00-30
Pages
13391-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC60881
Subset
IM
Grants
NIA NIH HHS · P01 AG014751 · United States
NIA NIH HHS · AG14751 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]