Ampakines promote spine actin polymerization, long-term potentiation, and learning in a mouse model of Angelman syndrome

Neurobiology of Disease

Volumn 47, Issue 2, 2012, Pages 210-215

  Baudry, Michel ^a   Kramar, Eniko ^b   Xu, Xiaobo ^a   Zadran, Homera ^a   Moreno, Stephanie ^c   Lynch, Gary ^b   Gall, Christine ^b   Bi, Xiaoning ^c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Western University of Health Sciences   (United States)

Author keywords

Actin; AMPA receptor; Hippocampus; Learning and memory; LTP; UBE3A

Indexed keywords

ACTIN; AMPA RECEPTOR AGONIST; AMPAKINE; CX 929; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONDITIONING; CONTROLLED STUDY; CYTOSKELETON; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; FEAR; FEAR CONDITIONING; GENE; HAPPY PUPPET SYNDROME; HIPPOCAMPAL CA1 REGION; LEARNING; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; THETA BURST STIMULATION; UBE3A GENE;

ACTINS; ANGELMAN SYNDROME; ANIMALS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MALE; MICE; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; POLYMERIZATION; RECEPTORS, AMPA; SPINAL CORD; UBIQUITIN-PROTEIN LIGASES;

EID: 84861656442     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.04.002     Document Type: Article

References (27)

1. Arai A.C., Kessler M. Pharmacology of ampakine modulators: from AMPA receptors to synapses and behavior. Curr. Drug Targets 2007, 8:583-602.
2. Baudry M., Bi X., Gall C., Lynch G. The biochemistry of memory: the 26-year journey of a 'new and specific hypothesis'. Neurobiol. Learn. Mem. 2011, 95:125-133.
3. Bramham C.R., Worley P.F., Moore M.J., Guzowski J.F. The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 2008, 28:11760-11767.
4. Dindot S.V., Antalffy B.A., Bhattacharjee M.B., Beaudet A.L. The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum. Mol. Genet. 2008, 17:111-118.
5. Greer P.L., Hanayama R., Bloodgood B.L., Mardinly A.R., Lipton D.M., Flavell S.W., Kim T.K., Griffith E.C., Waldon Z., Maehr R., Ploegh H.L., Chowdhury S., Worley P.F., Steen J., Greenberg M.E. The Angelman syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell 2010, 140:704-716.
6. Hamlyn E., Brand L., Shahid M., Harvey B.H. The ampakine, Org 26576, bolsters early spatial reference learning and retrieval in the Morris water maze: a subchronic, dose-ranging study in rats. Behav. Pharmacol. 2009, 20:662-667.
7. Jiang Y.H., Armstrong D., Albrecht U., Atkins C.M., Noebels J.L., Eichele G., Sweatt J.D., Beaudet A.L. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 1998, 21:799-811.
8. Kramar E.A., Lin B., Rex C.S., Gall C.M., Lynch G. Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5579-5584.
9. Kramar E.A., Chen L.Y., Lauterborn J.C., Simmons D.A., Gall C.M., Lynch G. BDNF upregulation rescues synaptic plasticity in middle-aged ovariectomized rats. Neurobiol. Aging 2012, 33:708-719.
10. Krause M., Yang Z., Rao G., Houston F.P., Barnes C.A. Altered dendritic integration in hippocampal granule cells of spatial learning-impaired aged rats. J. Neurophysiol. 2008, 99:2769-2778.
11. Kung V.W., Hassam R., Morton A.J., Jones S. Dopamine-dependent long term potentiation in the dorsal striatum is reduced in the R6/2 mouse model of Huntington's disease. Neuroscience 2007, 146:1571-1580.
12. Lalande M., Calciano M.A. Molecular epigenetics of Angelman syndrome. Cell. Mol. Life Sci. 2007, 64:947-960.
13. Lin B., Kramar E.A., Bi X., Brucher F.A., Gall C.M., Lynch G. Theta stimulation polymerizes actin in dendritic spines of hippocampus. J. Neurosci. 2005, 25:2062-2069.
14. Lynch G., Gall C.M. Ampakines and the threefold path to cognitive enhancement. Trends Neurosci. 2006, 29:554-562.
15. Lynch G., Kramar E.A., Rex C.S., Jia Y., Chappas D., Gall C.M., Simmons D.A. Brain-derived neurotrophic factor restores synaptic plasticity in a knock-in mouse model of Huntington's disease. J. Neurosci. 2007, 27:4424-4434.
16. Lynch G., Rex C.S., Chen L.Y., Gall C.M. The substrates of memory: defects, treatments, and enhancement. Eur. J. Pharmacol. 2008, 585:2-13.
17. Margolis S.S., Salogiannis J., Lipton D.M., Mandel-Brehm C., Wills Z.P., Mardinly A.R., Hu L., Greer P.L., Bikoff J.B., Ho H.Y., Soskis M.J., Sahin M., Greenberg M.E. EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation. Cell 2010, 143:442-455.
18. Nawaz Z., Lonard D.M., Smith C.L., Lev-Lehman E., Tsai S.Y., Tsai M.J., O'Malley B.W. The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol. Cell. Biol. 1999, 19:1182-1189.
19. Oliver C., Horsler K., Berg K., Bellamy G., Dick K., Griffiths E. Genomic imprinting and the expression of affect in Angelman syndrome: what's in the smile?. J. Child Psychol. Psychiatry 2007, 48:571-579.
20. Rex C.S., Lauterborn J.C., Lin C.Y., Kramár E.A., Rogers G.A., Gall C.M., Lynch G. Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J. Neurophysiol. 2006, 96:677-685.
21. Rex C.S., Lin C.Y., Kramar E.A., Chen L.Y., Gall C.M., Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J. Neurosci. 2007, 27:3017-3029.
22. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
23. Simmons D.A., Rex C.S., Palmer L., Pandyarajan V., Fedulov V., Gall C.M., Lynch G. Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4906-4911.
24. Simmons D.A., Mehta R.A., Lauterborn J.C., Gall C.M., Lynch G. Brief ampakine treatments slow the progression of Huntington's disease phenotypes in R6/2 mice. Neurobiol. Dis. 2011, 41:436-444.
25. van Woerden G.M., Harris K.D., Hojjati M.R., Gustin R.M., Qiu S., de Avila Freire R., Jiang Y.H., Elgersma Y., Weeber E.J. Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alphaCaMKII inhibitory phosphorylation. Nat. Neurosci. 2007, 10:280-282.
26. Williams C.A., Zori R.T., Stone J.W., Gray B.A., Cantu E.S., Ostrer H. Maternal origin of 15q11-13 deletions in Angelman syndrome suggests a role for genomic imprinting. Am. J. Med. Genet. 1990, 35:350-353.
27. Zheng Y., Balabhadrapatruni S., Masumura C., Darlington C.L., Smith P.F. Effects of the putative cognitive-enhancing ampakine, CX717, on attention and object recognition memory. Curr. Alzheimer Res. 2011, 8:876-882.