Estrogen-induced signaling attenuates soluble Aβ peptide-mediated dysfunction of pathways in synaptic plasticity

Brain Research

Volumn 1383, Issue , 2011, Pages 1-12

  Logan, Shaun M ^a   Sarkar, Saumyendra N ^a   Zhang, Zhang ^a   Simpkins, James W ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

17 estradiol; CaMKII; ERK; GluR1; Synaptic plasticity

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; ESTRADIOL; ESTROGEN; GLUTAMATE RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; OLIGOMER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN SLICE; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME ACTIVATION; ENZYME INHIBITION; ESTROGEN ACTIVITY; FEMALE; HIPPOCAMPUS; MEMORY; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; ESTRADIOL; ESTROGENS; FEMALE; NEURONAL PLASTICITY; PHOSPHORYLATION; RATS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 79952993427     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.01.038     Document Type: Article

References (52)

1. A. Barria, D. Muller, V. Derkach, L.C. Griffith, and T.R. Soderling Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation Science 276 1997 2042 2045 (Pubitemid 27443609)
2. J. Boehm, M.G. Kang, R.C. Johnson, J. Esteban, R.L. Huganir, and R. Malinow Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1 Neuron 51 2006 213 225 (Pubitemid 44041865)
3. M. Cammarota, R. Bernabeu, M. Levi De Stein, I. Izquierdo, and J.H. Medina Learning-specific, time-dependent increases in hippocampal Ca2+/calmodulin-dependent protein kinase II activity and AMPA GluR1 subunit immunoreactivity Eur. J. Neurosci. 10 1998 2669 2676
4. S. Connor, P.T. Williams, B. Armstrong, T.L. Petit, T.L. Ivanco, and A.C. Weeks Long-term potentiation is associated with changes in synaptic ultrastructure in the rat neocortex Synapse 59 2006 378 382
5. D.A. Cordoba Montoya, and H.F. Carrer Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats Brain Res. 778 1997 430 438 (Pubitemid 28037427)
6. F. Engert, and T. Bonhoeffer Dendritic spine changes associated with hippocampal long-term synaptic plasticity Nature 399 1999 66 70
7. J.A. Esteban, S.H. Shi, C. Wilson, M. Nuriya, R.L. Huganir, and R. Malinow PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity Nat. Neurosci. 6 2003 136 143 (Pubitemid 36182782)
8. M.R. Foy, J. Xu, X. Xie, R.D. Brinton, R.F. Thompson, and T.W. Berger 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation J. Neurophysiol. 81 1999 925 929 (Pubitemid 29264535)
9. B.H. Gahwiler Organotypic monolayer cultures of nervous tissue J. Neurosci. Methods 4 1981 329 342 (Pubitemid 12084147)
10. D. Grimm, A. Kern, K. Rittner, and J.A. Kleinschmidt Novel tools for production and purification of recombinant adenoassociated virus vectors Hum. Gene Ther. 9 1998 2745 2760 (Pubitemid 29027018)
11. M. Ikeda, T. Nobuaki, M. Hideo, H. Yasushi, M. Gen, T. Tomokazu, T. Norio, K. Tetsuya, and K. Suguru Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons Brain Res. Rev. 57 2008 363 375 (Pubitemid 351381769)
12. K.B. Jelks, R. Wylie, C.L. Floyd, A. Kimberly McAllister, and Phyllis Wise Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-α J. Neurosci. 27 2007 6903 6913 (Pubitemid 47015894)
13. C.D. Kopec, B. Li, W. Wei, J. Boehm, and R. Malinow Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation J. Neurosci. 26 2006 2000 2009
14. M.P. Lambert, K.L. Viola, B.A. Chromy, L. Chang, T.E. Morgan, J. Yu, D.L. Venton, G.A. Krafft, C.E. Finch, and W.L. Klein Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies J. Neurochem. 79 2001 595 605 (Pubitemid 33029933)
15. H.K. Lee, M. Barbarosie, K. Kameyama, M.F. Bear, and R.L. Huganir Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity Nature 405 2000 955 959 (Pubitemid 30435052)
16. H.K. Lee, K. Takamiya, J.S. Han, H. Man, C.H. Kim, G. Rumbaugh, S. Yu, L. Ding, C. He, R.S. Petralia, R.J. Wenthold, M. Gallagher, and R.L. Huganir Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory Cell 112 2003 631 643 (Pubitemid 36331776)
17. S.J. Lee, C.R. Campomanes, P.T. Sikat, A.T. Greenfield, P.B. Allen, and B.S. McEwen Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner Neuroscience 124 2004 549 560 (Pubitemid 38251323)
18. S.J. Lee, Y. Escobedo-Lozoya, E.M. Szatmari, and R. Yasuda Activation of CaMKII in single dendritic spines during long-term potentiation Nature 458 2009 299 304
19. D. Liao, R.H. Scannevin, and R. Huganir Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors J. Neurosci. 21 2001 6008 6017 (Pubitemid 32737734)
20. F. Liu, M. Day, L. Muñiz, D. Bitran, R. Arias, R. Revilla-Sanchez, S. Grauer, G. Zhang, C. Kelley, V. Pulito, A. Sung, R.F. Mervis, R. Navarra, W.D. Hirst, P.H. Reinhart, K.L. Marquis, S.J. Moss, M.N. Pangalos, and N.J. Brandon Activation of estrogen receptor-β regulates hippocampal synaptic plasticity and improves memory Nat. Neurosci. 11 2008 334 343 (Pubitemid 351311804)
21. A. Lu, R. Ran, S. Parmentier-Batteur, A. Nee, and F.R. Sharp Geldanamycin induces heat shock proteins in brain and protects against focal cerebral ischemia J. Neurochem. 81 2002 355 364 (Pubitemid 34809361)
22. W. Lu, H. Man, W. Ju, W.S. Trimble, J.F. MacDonald, and Y.T. Wang Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons Neuron 29 2001 243 254 (Pubitemid 32108736)
23. R. Malinow, and R.C. Malenka AMPA receptor trafficking and synaptic plasticity Annu. Rev. Neurosci. 25 2002 103 126 (Pubitemid 34748013)
24. E. Marder, and V. Thirumalai Cellular, synaptic and network effects of neuromodulation Neural Netw. 15 2002 479 493 (Pubitemid 34947459)
25. M. Matsuzaki, N. Honkura, G.C. Ellis-Davies, and H. Kasai Structural basis of long-term potentiation in single dendritic spines Nature 429 2004 761 766 (Pubitemid 38833127)
26. U.V. Nagerl, N. Eberhorn, S.B. Cambridge, and T. Bonhoeffer Bidirectional activity-dependent morphological plasticity in hippocampal neurons Neuron 44 2004 759 767 (Pubitemid 39575630)
27. K. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity Nat. Neurosci. 7 2004 1104 1112 (Pubitemid 41184451)
28. J.C. Poncer, J.A. Esteban, and R. Malinow Multiple mechanisms for the potentiation of AMPA receptor-mediated transmission by alpha-Ca2+/calmodulin- dependent protein kinase II J. Neurosci. 22 2002 4406 4411 (Pubitemid 37465657)
29. T.F. Roberts, K.A. Tschida, M.E. Klein, and R. Mooney Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning Nature 463 2010 948 952
30. K.W. Roche, R.J. O'Brien, A.L. Mammen, J. Bernhardt, and R.L. Huganir Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit Neuron 16 1996 1179 1188 (Pubitemid 26227239)
31. S.N. Sarkar, R.Q. Huang, S.M. Logan, K.D. Yi, G.H. Dillon, and J.W. Simpkins Estrogens directly potentiate neuronal L-type Ca2+ channels Proc. Natl Acad. Sci. USA 105 2008 15148 15153
32. T. Sawai, F. Bernier, T. Fukushima, T. Hashimoto, H. Ogura, and Y. Nishizawa Estrogen induces a rapid increase of calcium-calmodulin-dependent protein kinase II activity in the hippocampus Brain Res. 950 2002 308 311 (Pubitemid 35253944)
33. J.M. Schwarz, S.L. Liang, S.M. Thompson, and M.M. McCarthy Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences Neuron 58 2008 584 598 (Pubitemid 351672351)
34. G.M. Shankar, B.L. Bloodgood, M. Townsend, D.M. Walsh, D.J. Selkoe, and B.L. Sabatini Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway J. Neurosci. 27 2007 2866 2875 (Pubitemid 46438992)
35. G.M. Shankar, S. Li, T.H. Mehta, A. Garcia-Munoz, N.E. Shepardson, I. Smith, F.M. Brett, M.A. Farrell, M.J. Rowan, C.A. Lemere, C.M. Regan, D.M. Walsh, B.L. Sabatini, and D.J. Selkoe Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14 2008 837 842
36. B.R. Shrestha, O.V. Vitolo, P. Joshi, T. Lordkipanidze, M. Shelanski, and A. Dunaevsky Amyloid beta peptide adversely affects spine number and motility in hippocampal neurons Mol. Cell. Neurosci. 33 2006 274 282 (Pubitemid 44696319)
37. K.J. Sinopoli, S.B. Floresco, and L.A. Galea Systemic and local administration of estradiol into the prefrontal cortex or hippocampus differentially alters working memory Neurobiol. Learn. Mem. 86 2006 293 304 (Pubitemid 44436974)
38. E.M. Snyder, Y. Nong, C.G. Almeida, S. Paul, T. Moran, E.Y. Choi, A.C. Nairn, M.W. Salter, P.J. Lombroso, G.K. Gouras, and P. Greengard Regulation of NMDA receptor trafficking by amyloid-beta Nat. Neurosci. 8 2005 1051 1058 (Pubitemid 41061516)
39. I. Song, and R.L. Huganir Regulation of AMPA receptors during synaptic plasticity Trends Neurosci. 25 2002 578 588 (Pubitemid 35254182)
40. J.L. Spencer, E.M. Waters, R.D. Romeo, G.E. Wood, T.A. Milner, and B.S. McEwen Uncovering the mechanisms of estrogen effects on hippocampal function Front. Neuroendocrinol. 29 2008 219 237
41. T. Takahashi, K. Svoboda, and R. Malinow Experience strengthening transmission by driving AMPA receptors into synapses Science 299 2003 1585 1588 (Pubitemid 36297710)
42. Y. Takumi, V. Ramirez-Leon, P. Laake, E. Rinvik, and O.P. Ottersen Different modes of expression of AMPA and NMDA receptors in hippocampal synapses Nat. Neurosci. 2 1999 618 624 (Pubitemid 30491212)
43. R.D. Terry, E. Masliah, D.P. Salmon, N. Butters, R. DeTeresa, R. Hill, L.A. Hansen, and R. Katzman Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann. Neurol. 30 1991 572 580
44. M. Townsend, T. Mehta, and D.J. Selkoe Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway J. Biol. Chem. 282 2007 33305 33312 (Pubitemid 350159548)
45. J.R. Whitlock, A.J. Heynen, M.G. Shuler, and M.F. Bear Learning induces long-term potentiation in the hippocampus Science 313 2006 1093 1097 (Pubitemid 44300229)
46. C.S. Woolley Acute effects of estrogen on neuronal physiology Annu. Rev. Pharmacol. Toxicol. 47 2007 657 680
47. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: A potential initiation mechanism for estrogen-induced neuroprotection Neuroscience 135 2005 59 72 (Pubitemid 41219738)
48. J.G. Yague, A.C. Wang, W.G. Janssen, P.R. Hof, L.M. Garcia-Segura, I. Azcoitia, and J.H. Morrison Aromatase distribution in the monkey temporal neocortex and hippocampus Brain Res. 1209 2008 115 127
49. S.H. Yang, R. Liu, S.S. Wu, and J.W. Simpkins The use of estrogens and related compounds in the treatment of damage from cerebral ischemia Ann. NY Acad. Sci. 1007 2003 101 107 (Pubitemid 38253658)
50. S.-H. Yang, S.N. Sarkar, R. Liu, E.J. Perez, X. Wang, Y. Wen, L.J. Yan, and J.W. Simpkins Estrogen Receptor β as a Mitochondrial Vulnerability Factor J. Biol. Chem. 284 2009 9540 9548
51. D. Zhao, J.B. Watson, and C.W. Xie Amyloid beta prevents activation of calcium/calmodulin-dependent protein kinase II and AMPA receptor phosphorylation during hippocampal long-term potentiation J. Neurophysiol. 92 2004 2853 2858 (Pubitemid 40340496)
52. S. Zolotukhin, B.J. Byrne, E. Mason, I. Zolotukhin, M. Potter, K. Chesnut, C. Summerford, R.J. Samulski, and N. Muzyczka Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield Gene Ther. 6 1999 973 985 (Pubitemid 29295202)