Home LiteratureArticle Details
PMID: 18294775 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus.

Neuroscience ·Vol. 152 ·No. 2 ·2008-03-18 ·Pages 360-70

Yildirim M, Janssen WG, Tabori NE, Adams MM, Yuen GS, Akama KT, McEwen BS, Milner TA, Morrison JH

Abstract

17beta-Estradiol (E) increases axospinous synapse density in the hippocampal CA1 region of young female rats, but not in aged rats. This may be linked to age-related alterations in signaling pathways activated by synaptic estrogen receptor alpha (ER-alpha) that potentially regulate spine formation, such as LIM-kinase (LIMK), an actin depolymerizing factor/cofilin kinase. We hypothesized that, as with ER-alpha, phospho-LIM-kinase (pLIMK) may be less abundant or responsive to E in CA1 synapses of aged female rats. To address this, cellular and subcellular distribution of pLIMK-immunoreactivity (IR) in CA1 was analyzed by light and electron microscopy in young and aged female rats that were ovariectomized and treated with either vehicle or E. pLIMK-IR was found primarily in perikarya within the pyramidal cell layer and dendritic shafts and spines in stratum radiatum (SR). While pLIMK-IR was occasionally present in terminals, post-embedding quantitative analysis of SR showed that pLIMK had a predominant post-synaptic localization and was preferentially localized within the postsynaptic density (PSD). The percentage of pLIMK-labeled synapses increased (30%) with E treatment (P<0.02) in young animals, and decreased (43%) with age (P<0.002) regardless of treatment. The pattern of distribution of pLIMK-IR within dendritic spines and synapses was unaffected by age or E treatment, with the exception of an E-induced increase in the non-synaptic core of spines in young females. These data suggest that age-related synaptic alterations similar to those seen with ER-alpha occur with signaling molecules such as pLIMK, and support the hypothesis that age-related failure of E treatment to increase synapse number in CA1 may be due to changes in the molecular profile of axospinous synapses with respect to signaling pathways linked to formation of additional spines and synapses in response to E.

MeSH Terms
Age Factors Aging/physiology Animals Estradiol/pharmacology Estrogen Receptor alpha/metabolism Estrogens/pharmacology Female Hippocampus/cytology,drug effects Lim Kinases/metabolism Microscopy, Immunoelectron/methods Ovariectomy Phosphorylation Rats Rats, Sprague-Dawley Synapses/drug effects,enzymology,ultrastructure
Chemicals
Estrogen Receptor alpha Estrogens Estradiol Lim Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Yildirim M
Department of Pharmacology, Hacettepe University, Faculty of Medicine, Ankara, Turkey.
Janssen W G M
Tabori N E
Adams M M
Yuen G S
Akama K T
McEwen B S
Milner T A
Morrison J H
References (58)
58 references, click to expand
  1. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo.
    Neuron. 2003 May 8;38(3):447-60 PMID: 12741991
  2. Association of p53 and MSH2 with recombinative repair complexes during S phase.
    Oncogene. 2002 Jul 18;21(31):4788-800 PMID: 12101417
  3. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus.
    Eur J Neurosci. 1996 Jul;8(7):1488-500 PMID: 8758956
  4. Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin.
    J Neurosci. 2003 Apr 1;23(7):2527-37 PMID: 12684437
  5. Changes in neurotensin mRNA by estrogen in the female rat preoptic area during aging: an in situ hybridization histochemistry study.
    Gen Comp Endocrinol. 1998 Dec;112(3):364-71 PMID: 9843642
  6. LIM-kinase 2 and cofilin phosphorylation mediate actin cytoskeleton reorganization induced by transforming growth factor-beta.
    J Biol Chem. 2005 Mar 25;280(12):11448-57 PMID: 15647284
  7. Sequence requirements for estrogen receptor binding to estrogen response elements.
    J Biol Chem. 1998 Nov 6;273(45):29321-30 PMID: 9792632
  8. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1.
    J Cell Biol. 2003 Sep 15;162(6):1089-98 PMID: 12963706
  9. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility.
    J Cell Biol. 1997 Mar 24;136(6):1307-22 PMID: 9087445
  10. Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory.
    Neuroendocrinology. 2006;84(4):255-63 PMID: 17142999
  11. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats.
    Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):8071-6 PMID: 11427724
  12. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin.
    J Cell Biol. 2007 Jul 2;178(1):107-19 PMID: 17606869
  13. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin.
    J Biol Chem. 2005 Apr 1;280(13):12683-9 PMID: 15671020
  14. Length of postovariectomy interval and age, but not estrogen replacement, regulate N-methyl-D-aspartate receptor mRNA levels in the hippocampus of female rats.
    Exp Neurol. 2001 Aug;170(2):345-56 PMID: 11476600
  15. Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus.
    J Comp Neurol. 2004 Jun 28;474(3):419-26 PMID: 15174084
  16. Regulation of spine morphology and synaptic function by LIMK and the actin cytoskeleton.
    Rev Neurosci. 2003;14(3):233-40 PMID: 14513866
  17. Head, neck, and spines: a role for LIMK-1 in the hippocampus.
    Neuron. 2002 Jul 3;35(1):3-5 PMID: 12123600
  18. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats.
    J Neurosci. 2002 May 1;22(9):3608-14 PMID: 11978836
  19. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons.
    J Neurochem. 2007 Feb;100(4):950-67 PMID: 17266735
  20. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood.
    J Neurosci. 1990 Apr;10(4):1286-91 PMID: 2329377
  21. Contribution of cytoskeleton to the internalization of AMPA receptors.
    Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):1261-6 PMID: 11158627
  22. Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens.
    J Histochem Cytochem. 1991 Sep;39(9):1267-79 PMID: 1833448
  23. Vitamin D and gonadal steroid-resistant New World primate cells express an intracellular protein which competes with the estrogen receptor for binding to the estrogen response element.
    J Clin Invest. 1997 Feb 15;99(4):669-75 PMID: 9045869
  24. N-methyl-D-aspartate receptor mRNA levels change during reproductive senescence in the hippocampus of female rats.
    Exp Neurol. 2001 Jul;170(1):171-9 PMID: 11421594
  25. Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus.
    Hippocampus. 2006;16(5):453-63 PMID: 16526034
  26. P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-alpha and promotes hyperplasia in mammary epithelium.
    EMBO J. 2002 Oct 15;21(20):5437-47 PMID: 12374744
  27. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase.
    Nature. 1998 Jun 25;393(6687):805-9 PMID: 9655397
  28. Signal-regulated ADF/cofilin activity and growth cone motility.
    Mol Neurobiol. 2000 Feb-Apr;21(1-2):97-107 PMID: 11327152
  29. Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails.
    J Cell Biol. 1997 Mar 24;136(6):1323-32 PMID: 9087446
  30. Estradiol induction of proenkephalin messenger RNA in hypothalamus: dose-response and relation to reproductive behavior in the female rat.
    Brain Res Mol Brain Res. 1990 Jun;8(1):47-54 PMID: 2166200
  31. Potentiation of human estrogen receptor alpha transcriptional activation through phosphorylation of serines 104 and 106 by the cyclin A-CDK2 complex.
    J Biol Chem. 1999 Aug 6;274(32):22296-302 PMID: 10428798
  32. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice.
    Neuron. 2002 Jul 3;35(1):121-33 PMID: 12123613
  33. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization.
    Nature. 1998 Jun 25;393(6687):809-12 PMID: 9655398
  34. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat.
    J Neurosci. 1992 Jul;12(7):2549-54 PMID: 1613547
  35. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase.
    Science. 1999 Aug 6;285(5429):895-8 PMID: 10436159
  36. Spine architecture and synaptic plasticity.
    Trends Neurosci. 2005 Apr;28(4):182-7 PMID: 15808352
  37. 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. 1999 Apr;32(2):93-122 PMID: 10337493
  38. Proteins of the ADF/cofilin family: essential regulators of actin dynamics.
    Annu Rev Cell Dev Biol. 1999;15:185-230 PMID: 10611961
  39. Evidence that long-term potentiation occurs within individual hippocampal synapses during learning.
    J Neurosci. 2007 Jul 25;27(30):8031-9 PMID: 17652593
  40. Cellular and synaptic distribution of NR2A and NR2B in macaque monkey and rat hippocampus as visualized with subunit-specific monoclonal antibodies.
    Exp Neurol. 2005 Feb;191 Suppl 1:S28-44 PMID: 15629759
  41. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses.
    Neuron. 2004 Dec 2;44(5):749-57 PMID: 15572107
  42. Estrogen regulation of Pak1 and FKHR pathways in breast cancer cells.
    FEBS Lett. 2003 Jan 30;535(1-3):6-10 PMID: 12560069
  43. A Drosophila homolog of LIM-kinase phosphorylates cofilin and induces actin cytoskeletal reorganization.
    Biochem Biophys Res Commun. 2000 Oct 5;276(3):1178-85 PMID: 11027607
  44. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics.
    Nat Cell Biol. 1999 Sep;1(5):253-9 PMID: 10559936
  45. Identification and characterization of a novel family of serine/threonine kinases containing two N-terminal LIM motifs.
    J Biol Chem. 1995 Dec 29;270(52):31321-30 PMID: 8537403
  46. Regulation of the neuronal actin cytoskeleton by ADF/cofilin.
    J Neurobiol. 2004 Jan;58(1):103-17 PMID: 14598374
  47. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity.
    Nat Neurosci. 2004 Oct;7(10):1104-12 PMID: 15361876
  48. Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase.
    J Biol Chem. 2001 Jan 5;276(1):670-6 PMID: 11018042
  49. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats.
    J Comp Neurol. 1997 Dec 1;388(4):603-12 PMID: 9388019
  50. Role for Hsp90-associated cochaperone p23 in estrogen receptor signal transduction.
    Mol Cell Biol. 1999 May;19(5):3748-59 PMID: 10207098
  51. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop.
    J Biol Chem. 2000 Feb 4;275(5):3577-82 PMID: 10652353
  52. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites.
    J Comp Neurol. 2001 Jan 15;429(3):355-71 PMID: 11116225
  53. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha.
    J Neurosci. 2007 Jun 27;27(26):6903-13 PMID: 17596438
  54. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat.
    J Comp Neurol. 1996 Sep 09;373(1):108-17 PMID: 8876466
  55. Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase.
    Neuropharmacology. 2004 Oct;47(5):746-54 PMID: 15458846
  56. Spatial organization of cofilin in dendritic spines.
    Neuroscience. 2006;138(2):447-56 PMID: 16388910
  57. Beta estrogen receptor knockout (BERKO) mice present attenuated hippocampal CA1 long-term potentiation and related memory deficits in contextual fear conditioning.
    Behav Brain Res. 2005 Oct 14;164(1):128-31 PMID: 16054246
  58. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation.
    J Comp Neurol. 2005 Oct 17;491(2):81-95 PMID: 16127691
Article Info
Journal
Neuroscience
Abbr.
Neuroscience
ISSN
0306-4522
Published
2008-03-18
Epub
2008-00-12
Pages
360-70
Language
English
Region
United States
NLM ID
7605074
PMCID
PMC2396523
Subset
IM
Grants
NIA NIH HHS · P01 AG016765 · United States
NINDS NIH HHS · R01 NS007080 · United States
NINDS NIH HHS · NS07080 · United States
NIA NIH HHS · P01-AG16765 · 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]