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

Neuroscience

Volumn 152, Issue 2, 2008, Pages 360-370

  Yildirim, M ^a,b,c   Janssen, W G M ^b   Tabori, N E ^c,d   Adams, M M ^e   Yuen, G S ^c   Akama, K T ^c   McEwen, B S ^c   Milner, T A ^c,d   Morrison, J H ^b  

^a HACETTEPE UNIVERSITY   (Turkey)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

electron microscopy; immunogold; plasticity; sex steroids; signal transduction; synapse

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; LIM KINASE; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME PHOSPHORYLATION; FEMALE; HIPPOCAMPUS; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

AGE FACTORS; AGING; ANIMALS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HIPPOCAMPUS; LIM KINASES; MICROSCOPY, IMMUNOELECTRON; OVARIECTOMY; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 40949153802     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.01.004     Document Type: Article

References (61)

1. Adams M.M., Fink S.E., Janssen W.G., Shah R.A., and Morrison J.H. Estrogen modulates synaptic N-methyl-d-aspartate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474 (2004) 419-426
2. Adams M.M., Fink S.E., Shah R.A., Janssen W.G., Hayashi S., Milner T.A., McEwen B.S., and Morrison J.H. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 22 (2002) 3608-3614
3. Adams M.M., Morrison J.H., and Gore A.C. N-methyl-D-aspartate receptor mRNA levels change during reproductive senescence in the hippocampus of female rats. Exp Neurol 170 (2001) 171-179
4. Adams M.M., Oung T., Morrison J.H., and Gore A.C. 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 170 (2001) 345-356
5. Adams M.M., Shah R.A., Janssen W.G., and Morrison J.H. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci U S A 98 (2001) 8071-8076
6. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., and Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393 (1998) 805-809
7. Bamburg J.R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15 (1999) 185-230
8. Carlier M.F., Laurent V., Santolini J., Melki R., Didry D., Xia G.X., Hong Y., Chua N.H., and Pantaloni D. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136 (1997) 1307-1322
9. Carlisle H.J., and Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci 28 (2005) 182-187
10. Chen H., Arbelle J.E., Gacad M.A., Allegretto E.A., and Adams J.S. 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 99 (1997) 669-675
11. Day M., Sung A., Logue S., Bowlby M., and Arias R. Beta estrogen receptor knockout (BERKO) mice present attenuated hippocampal CA1 long-term potentiation and related memory deficits in contextual fear conditioning. Behav Brain Res 164 (2005) 128-131
12. Driscoll M.D., Sathya G., Muyan M., Klinge C.M., Hilf R., and Bambara R.A. Sequence requirements for estrogen receptor binding to estrogen response elements. J Biol Chem 273 (1998) 29321-29330
13. Edwards D.C., Sanders L.C., Bokoch G.M., and Gill G.N. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1 (1999) 253-259
14. Endo M., Ohashi K., Sasaki Y., Goshima Y., Niwa R., Uemura T., and Mizuno K. Control of growth cone motility and morphology by LIM kinase and slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 23 (2003) 2527-2537
15. Fedulov V., Rex C.S., Simmons D.A., Palmer L., Gall C.M., and Lynch G. Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. J Neurosci 27 (2007) 8031-8039
16. Foletta V.C., Lim M.A., Soosairajah J., Kelly A.P., Stanley E.G., Shannon M., He W., Das S., Massague J., and Bernard O. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J Cell Biol 162 (2003) 1089-1098
17. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., and Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38 (2003) 447-460
18. Funabashi T., Kleopoulos S.P., Kimura F., and Mobbs C.V. Changes in neurotensin mRNA by estrogen in the female rat preoptic area during aging: an in situ hybridization histochemistry study. Gen Comp Endocrinol 112 (1998) 364-371
19. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990) 1286-1291
20. Janssen W.G., Vissavajjhala P., Andrews G., Moran T., Hof P.R., and Morrison J.H. Cellular and synaptic distribution of NR2A and NR2B in macaque monkey and rat hippocampus as visualized with subunit-specific monoclonal antibodies. Exp Neurol 191 Suppl 1 (2005) S28-S44
21. Jelks K.B., Wylie R., Floyd C.L., McAllister A.K., and Wise P. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha. J Neurosci 27 (2007) 6903-6913
22. Knoblauch R., and Garabedian M.J. Role for Hsp90-associated cochaperone p23 in estrogen receptor signal transduction. Mol Cell Biol 19 (1999) 3748-3759
23. Lauber A.H., Romano G.J., Mobbs C.V., Howells R.D., and Pfaff D.W. 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 (1990) 47-54
24. Leranth C., and Pickel V.M. Electron microscopic preembedding double-labeling methods. In: Heimer L., and Zaborszky L. (Eds). Neuroanatomical tract-tracing methods (1989), Plenum Press, New York 129-172
25. Lujan R., Nusser Z., Roberts J.D., Shigemoto R., and Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8 (1996) 1488-1500
26. Maekawa M., Ishizaki T., Boku S., Watanabe N., Fujita A., Iwamatsu A., Obinata T., Ohashi K., Mizuno K., and Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285 (1999) 895-898
27. Mazumdar A., and Kumar R. Estrogen regulation of Pak1 and FKHR pathways in breast cancer cells. FEBS Lett 535 (2003) 6-10
28. Meberg P.J. Signal-regulated ADF/cofilin activity and growth cone motility. Mol Neurobiol 21 (2000) 97-107
29. Meng Y., Takahashi H., Meng J., Zhang Y., Lu G., Asrar S., Nakamura T., and Jia Z. Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase. Neuropharmacology 47 (2004) 746-754
30. Meng Y., Zhang Y., Tregoubov V., Falls D.L., and Jia Z. Regulation of spine morphology and synaptic function by LIMK and the actin cytoskeleton. Rev Neurosci 14 (2003) 233-240
31. Meng Y., Zhang Y., Tregoubov V., Janus C., Cruz L., Jackson M., Lu W.Y., MacDonald J.F., Wang J.Y., Falls D.L., and Jia Z. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35 (2002) 121-133
32. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491 (2005) 81-95
33. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., and Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429 (2001) 355-371
34. Mukai H., Tsurugizawa T., Murakami G., Kominami S., Ishii H., Ogiue-Ikeda M., Takata N., Tanabe N., Furukawa A., Hojo Y., Ooishi Y., Morrison J.H., Janssen W.G., Rose J.A., Chambon P., Kato S., Izumi S., Yamazaki T., Kimoto T., and Kawato S. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem 100 (2007) 950-967
35. Mukai H., Tsurugizawa T., Ogiue-Ikeda M., Murakami G., Hojo Y., Ishii H., Kimoto T., and Kawato S. Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory. Neuroendocrinology 84 (2006) 255-263
36. Ohashi K., Hosoya T., Takahashi K., Hing H., and Mizuno K. A Drosophila homolog of LIM-kinase phosphorylates cofilin and induces actin cytoskeletal reorganization. Biochem Biophys Res Commun 276 (2000) 1178-1185
37. Ohashi K., Nagata K., Maekawa M., Ishizaki T., Narumiya S., and Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275 (2000) 3577-3582
38. Okamoto K., Nagai T., Miyawaki A., and Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7 (2004) 1104-1112
39. Okano I., Hiraoka J., Otera H., Nunoue K., Ohashi K., Iwashita S., Hirai M., and Mizuno K. Identification and characterization of a novel family of serine/threonine kinases containing two N-terminal LIM motifs. J Biol Chem 270 (1995) 31321-31330
40. Peters A., Palay S.L., and Webster H. The fine structure of the nervous system: neurons and their supporting cells. 3rd edition (1991), Oxford University Press Inc, New York
41. Racz B., and Weinberg R.J. Spatial organization of cofilin in dendritic spines. Neuroscience 138 (2006) 447-456
42. Rogatsky I., Trowbridge J.M., and Garabedian M.J. Potentiation of human estrogen receptor alpha transcriptional activation through phosphorylation of serines 104 and 106 by the cyclin A-CDK2 complex. J Biol Chem 274 (1999) 22296-22302
43. Rosenblatt J., Agnew B.J., Abe H., Bamburg J.R., and Mitchison T.J. Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J Cell Biol 136 (1997) 1323-1332
44. Ruud H.K., and Blackstad T.W. 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 (1999) 93-122
45. Sarmiere P.D., and Bamburg J.R. Head, neck, and spines: a role for LIMK-1 in the hippocampus. Neuron 35 (2002) 3-5
46. Sarmiere P.D., and Bamburg J.R. Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol 58 (2004) 103-117
47. Sumi T., Matsumoto K., and Nakamura T. Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase. J Biol Chem 276 (2001) 670-676
48. Szymczak S., Kalita K., Jaworski J., Mioduszewska B., Savonenko A., Markowska A., Merchenthaler I., and Kaczmarek L. Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus. Hippocampus 16 (2006) 453-463
49. van Lookeren Campagne M., Oestreicher A.B., van der Krift T.P., Gispen W.H., and Verkleij A.J. Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J Histochem Cytochem 39 (1991) 1267-1279
50. Vardouli L., Moustakas A., and Stournaras C. LIM-kinase 2 and cofilin phosphorylation mediate actin cytoskeleton reorganization induced by transforming growth factor-beta. J Biol Chem 280 (2005) 11448-11457
51. Wang R.A., Mazumdar A., Vadlamudi R.K., and Kumar R. P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-alpha and promotes hyperplasia in mammary epithelium. EMBO J 21 (2002) 5437-5447
52. Wang Y., Shibasaki F., and Mizuno K. Calcium signal-induced cofilin dephosphorylation is mediated by slingshot via calcineurin. J Biol Chem 280 (2005) 12683-12689
53. Weiland N.G., Orikasa C., Hayashi S., and McEwen B.S. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 388 (1997) 603-612
54. Wen Z., Han L., Bamburg J.R., Shim S., Ming G.L., and Zheng J.Q. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and slingshot phosphatase on ADF/cofilin. J Cell Biol 178 (2007) 107-119
55. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12 (1992) 2549-2554
56. Woolley C.S., Wenzel H.J., and Schwartzkroin P.A. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 373 (1996) 108-117
57. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., and Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393 (1998) 809-812
58. Yuen G.S., Akama K.T., and McEwen B.S. Estrogen regulation of actin dynamics: mechanism for dendritic spine remodeling. Soc Neurosci (2004) 72.5, Online
59. Zhou Q., Homma K.J., and Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44 (2004) 749-757
60. Zhou Q., Xiao M., and Nicoll R.A. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc Natl Acad Sci U S A 98 (2001) 1261-1266
61. Zink D., Mayr C., Janz C., and Wiesmuller L. Association of p53 and MSH2 with recombinative repair complexes during S phase. Oncogene 21 (2002) 4788-4800