7, 8-Dihydroxyflavone induces synapse expression of AMPA GluA1 and ameliorates cognitive and spine abnormalities in a mouse model of fragile X syndrome

Neuropharmacology

Volumn 89, Issue , 2015, Pages 43-53

  Tian, Mi ^a   Zeng, Yan ^a   Hu, Yilan ^a   Yuan, Xiuxue ^a   Liu, Shumin ^a   Li, Jie ^a   Lu, Pan ^a   Sun, Yao ^a   Gao, Lei ^a   Fu, Daan ^a   Li, Yi ^a   Wang, Shasha ^a   McClintock, Shawn M ^b,c  

^a WUHAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

7 8 Dihydroxyflavone; AMPA receptor; BDNF; Fragile X syndrome; TrkB agonist

Indexed keywords

7,8 DIHYDROXYFLAVONE; AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; FRAGILE X MENTAL RETARDATION PROTEIN; GLUA1 RECEPTOR; PROTEIN KINASE C; SERINE; UNCLASSIFIED DRUG; 6,7-DIHYDROXYFLAVONE; FLAVONE DERIVATIVE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; DRUG EFFECT; DRUG MECHANISM; DRUG SYNTHESIS; FEAR; FMR1 GENE; FRAGILE X SYNDROME; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; SPINE MALFORMATION; ANIMAL; BIOSYNTHESIS; COGNITION DISORDERS; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SYNAPSE;

ANIMALS; COGNITION DISORDERS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; FLAVONES; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; RECEPTORS, AMPA; SYNAPSES;

EID: 84907936867     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.09.006     Document Type: Article

References (62)

1. S.J. Allen, J.J. Watson, and D. Dawbarn The neurotrophins and their role in Alzheimer's disease Curr. Neuropharmacol. 9 2011 559 573
2. B.K. Andrásfalvy, M.A. Smith, T. Borchardt, R. Sprengel, and J.C. Magee Impaired regulation of synaptic strength in hippocampal neurons from GluR1-deficient mice J. Physiol. 552 2003 35 45
3. C. Aoki, K. Wu, A. Elste, Gw Len, Sy Lin, G. McAuliffe, and I.B. Black Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex J. Neurosci. Res. 59 2000 454 463
4. M.F. Bear, K.M. Huber, and S.T. Warren The mGluR theory of fragile X mental retardation Trends Neurosci. 27 2004 370 377
5. M.V. Bell, M.C. Hirst, Y. Nakahori, R.N. MacKinnon, A. Roche, T.J. Flint, P.A. Jacobs, N. Tommerup, L. Tranebjaerg, and U. Froster-Iskenius Physical mapping across the fragile X: hypermethylation and clinical expression of the fragile X syndrome Cell 64 1991 861 866
6. E. Berry-Kravis, S.E. Krause, S.S. Block, S. Guter, J. Wuu, S. Leurgans, P. Decle, K. Potanos, E. Cook, J. Salt, D. Maino, D. Weinberg, R. Lara, T. Jardini, J. Cogswell, S.A. Johnson, and R. Hagerman Effect of CX516, an AMPA-modulating compound, on cognition and behavior in fragile X syndrome: a controlled trial J. Child Adolesc. Psychopharmacol. 16 2006 525 540
7. 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
8. M.V. Caldeira, C.V. Melo, D.B. Pereira, R. Carvalho, S.S. Correia, D.S. Backos, A.L. Carvalho, J.A. Esteban, and C.B. Duarte Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons J. Biol. Chem. 282 2007 12619 12628
9. J. Charbord, P. Poydenot, C. Bonnefond, M. Feyeux, F. Casagrande, B. Brinon, L. Francelle, G. Aurégan, M. Guillermier, M. Cailleret, P. Viegas, C. Nicoleau, C. Martinat, E. Brouillet, E. Cattaneo, M. Peschanski, M. Lechuga, and A.L. Perrier High throughput screening for inhibitors of REST in neural derivatives of human embryonic stem cells reveals a chemical compound that promotes expression of neuronal genes Stem Cells 31 2013 1816 1828
10. H.S. Crombag, J.M. Sutton, K. Takamiya, P.C. Holland, M. Gallagher, and R.L. Huganir A role for alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid GluR1 phosphorylation in the modulatory effects of appetitive reward cues on goal-directed behavior Eur. J. Neurosci. 27 2008 3284 3291
11. S. De Rubeis, and C. Bagni Regulation of molecular pathways in the Fragile X Syndrome: insights into Autism Spectrum Disorders J. Neurodev. Disord. 3 2011 257 269
12. R. D'Hooge, G. Nagels, F. Franck, C.E. Bakker, E. Reyniers, K. Storm, R.F. Kooy, B.A. Oostra, P.J. Willems, and P.P. De Deyn Mildly impaired water maze performance in male Fmr1 knockout mice Neuroscience 76 1997 367 376
13. C.T. Drake, T.A. Milner, and S.L. Patterson Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity J. Neurosci. 19 1999 8009 8026
14. J. Du, L. Feng, F. Yang, and B. Lu Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons J. Cell Biol. 150 2000 1423 1434
15. E. Engler-Chiurazzi, C. Tsang, S. Nonnenmacher, W.S. Liang, J.J. Corneveaux, L. Prokai, M.J. Huentelman, and H.A. Bimonte-Nelson Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats Neurobiol. Aging 32 2011 680 697
16. A.W. Grossman, G.M. Aldridge, K.J. Lee, M.K. Zeman, C.S. Jun, H.S. Azam, T. Arii, K. Imoto, W.T. Greenough, and I.J. Rhyu Developmental characteristics of dendritic spines in the dentate gyrus of Fmr1 knockout mice Brain Res. 1355 2010 221 227
17. A.R. Gomes, S.S. Correia, A.L. Carvalho, and C.B. Duarte Regulation of AMPA receptor activity, synaptic targeting and recycling: role in synaptic plasticity Neurochem. Res. 28 2003 1459 1473
18. Y. Hayashi, S.H. Shi, J.A. Esteban, A. Piccini, J.C. Poncer, and R. Malinow Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction Science 287 2000 2262 2267
19. C.X. He, and C. Portera-Cailliau The trouble with spines in fragile X syndrome: density, maturity and plasticity Neuroscience 251 2012 120 128
20. D. Hessl, S. Rivera, K. Koldewyn, L. Cordeiro, J. Adams, F. Tassone, P.J. Hagerman, and R.J. Hagerman Amygdala dysfunction in men with the fragile X premutation Brain 130 2007 404 416
21. L. Hou, M.D. Antion, D. Hu, C.M. Spencer, R. Paylor, and E. Klann Dynamic Translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression Neuron 51 2006 441 454
22. J.T. Isaac, M. Ashby, and C.J. McBain The role of the GluR2 subunit in AMPA Receptor function and synaptic plasticity Neuron 54 2007 859 871
23. S.W. Jang, X. Liu, M. Yepes, K.R. Shepherd, G.W. Miller, Y. Liu, W.D. Wilson, G. Xiao, B. Blanchi, Y.E. Sun, and K. Ye A selective TrkB agonist with potent neurotrophic activities by 7, 8-dihydroxyflavone Proc. Natl. Acad. Sci. U. S. A. 107 2010 2687 2692
24. M. Jiang, Q. Peng, X. Liu, J. Jin, Z. Hou, J. Zhang, S. Mori, C.A. Ross, K. Ye, and W. Duan Small-molecule TrkB receptor agonists improve motor function and extend survival in a mouse model of Huntington's disease Hum. Mol. Genet. 22 2013 2462 2470
25. H. Jourdi, and M. Kabbaj Acute BDNF treatment upregulates GluR1-SAP97 and GluR2-GRIP1 interactions: implications for sustained AMPA receptor expression PLoS One 8 2013 e57124
26. A. Kielland, G. Bochorishvili, J. Corson, L. Zhang, D.L. Rosin, P. Heggelund, and J.J. Zhu Activity patterns govern synapse-specific AMPA receptor trafficking between deliverable and synaptic pools Neuron 62 2009 84 101
27. S. Knafo, C. Venero, C. Sánchez-Puelles, I. Pereda-Peréz, A. Franco, C. Sandi, L.M. Suárez, J.M. Solís, L. Alonso-Nanclares, E.D. Martín, P. Merino-Serrais, E. Borcel, S. Li, Y. Chen, J. Gonzalez-Soriano, V. Berezin, E. Bock, J. Defelipe, and J.A. Esteban Facilitation of AMPA receptor synaptic delivery as a molecular mechanism for cognitive enhancement PLoS Biol. 10 2012 e1001262
28. J.C. Lauterborn, C.S. Rex, E. Kramar, L.Y. Chen, V. Pandyarajan, G. Lynch, and C.M. Gall Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome J. Neurosci. 27 2007 10685 10694
29. J.C. Lauterborn, M. Jafari, A.H. Babayan, and C.M. Gall Environmental enrichment reveals effects of genotype on hippocampal spine morphologies in the mouse model of fragile X syndrome Cereb. Cortex 2013 Sep 17 (Epub ahead of print)
30. G. Leal, D. Comprido, and C.B. Duarte BDNF-induced local protein synthesis and synaptic plasticity Neuropharmacology 76 2014 639 656
31. 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
32. H.K. Lee, and R.L. Huganir AMPA receptor regulation and the reversal of synaptic plasticity - LTP, LTD, depotentiation, and dedepression J.D. Sweatt, Learning and Memory: a Comprehensive Reference 2008 Elsevier Press
33. J. Levenga, F.M. de Vrij, B.A. Oostra, and R. Willemsen Potential Therapeutic interventions for fragile X syndrome Trends Mol. Med. 16 2010 516 527
34. L. Liao, S.K. Park, T. Xu, P. Vanderklish, and J.R. Yates 3rd Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice Proc. Natl. Acad. Sci. U. S. A. 105 2008 15281 15286
35. D.T. Lin, and R.L. Hugania PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization J. Neurosci. 27 2007 13903 13908
36. X. Liu, C.B. Chan, Q. Qi, G. Xiao, H.R. Luo, X. He, and K. Ye Optimization of a small tropomyosin-related kinase B (TrkB) agonist 7, 8-dihydroxyflavone active in mouse models of depression J. Med. Chem. 55 2012 8524 8537
37. V. Louhivuori, A. Vicario, M. Uutela, T. Rantam aki, L.M. Louhivuori, E. Castren, E. Tongiorgi, K.E. Akerman, and M.L. Castrén BDNF and TrkB in neuronal differentiation of Fmr1-knockout mouse Neurobiol. Dis. 41 2011 469 480
38. S. Moriguchi, N. Shioda, F. Han, J.Z. Yeh, T. Narahashi, and K. Fukunaga Galantamine enhancement of long-term potentiation is mediated by calcium/calmodulin-dependent protein kinase II and protein kinase C activation Hippocampus 19 2009 844 854
39. T.K. Murray, K. Whalley, C.S. Robinson, M.A. Ward, C.A. Hicks, D. Lodge, J.L. Vandergriff, P. Baumbarger, E. Siuda, M. Gates, A.M. Ogden, P. Skolnick, D.M. Zimmerman, E.S. Nisenbaum, D. Bleakman, and M.J. O'Neill LY503430, a novel alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor potentiator with functional, neuroprotective and neurotrophic effects in rodent models of Parkinson's disease J. Pharmacol. Exp. Ther. 306 2003 752 762
40. M. Nakamoto, V. Nalavadi, M.P. Epstein, U. Narayanan, G.J. Bassell, and S.T. Warren Fragile X mental retardation protein deficiency leads to excessive mGluR5-dependent internalization of AMPA receptors Proc. Natl. Acad. Sci. U. S. A. 104 2007 15537 15542
41. M. Narisawa-Saito, J. Carnahan, K. Araki, T. Yamaguchi, and H. Nawa Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons Neuroscience 88 1999 1009 1014
42. M. Narisawa-Saito, Y. Iwakura, M. Kawamura, K. Araki, S. Kozaki, N. Takei, and H. Nawa Brain-derived neurotrophic factor regulates surface expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethylmaleimide-sensitive factor/GluR2 interaction in developing neocortical neurons J. Biol. Chem. 277 2002 40901 40910
43. E.K. Osterweil, D.D. Krueger, K. Reinhold, and M.F. Bear Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome J. Neurosci. 30 2010 15616 15627
44. W. Paradee, H.E. Melikian, D.L. Rasmussen, A. Kenneson, P.J. Conn, and S.T. Warren Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function Neuroscience 94 1999 185 192
45. S. Park, J.M. Park, S. Kim, J.A. Kim, J.D. Shepherd, C.L. Smith-Hicks, S. Chowdhury, W. Kaufmann, D. Kuhl, A.G. Ryazanov, R.L. Huganir, D.J. Linden, and P.F. Worley Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD Neuron 59 2008 70 83
46. D.B. Pereira, N. Rebola, R.J. Rodrigues, R.A. Cunha, A.P. Carvalho, and C.B. Duarte TrkB receptors modulation of glutamate release is limited to a subset of nerve terminals in the adult rat hippocampus J. Neurosci. Res. 83 2006 832 844
47. A.S. Pop, J. Levenga, C.E. de Esch, R.A. Buijsen, I.M. Nieuwenhuizen, T. Li, A. Isaacs, F. Gasparini, B.A. Oostra, and R. Willemsen Rescue of dendritic spine phenotype in Fmr1 KO mice with the mGluR5 antagonist AFQ056/Mavoglurant Psychopharmacology (Berl) 231 2014 1227 1235
48. R.R. Seese, A.H. Babayan, A.M. Katz, C.D. Cox, J.C. Lauterborn, G. Lynch, and C.M. Gall LTP induction translocates cortactin at distant synapses in wild-type but not Fmr1 knock-out mice J. Neurosci. 32 2012 7403 7413
49. J.D. Shepherd, G. Rumbaugh, J. Wu, S. Chowdhury, N. Plath, D. Kuhl, R.L. Huganir, and P.F. Worley Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors Neuron 52 2006 475 484
50. M.E. Soden, and L. Chen Fragile X protein FMRP is required for homeostatic plasticity and regulation of synaptic strength by retinoic acid J. Neurosci. 30 2010 16910 16921
51. R.L. Stornetta, and J.J. Zhu Ras and Rap signaling in synaptic plasticity and mental disorders Neuroscientist 17 2011 54 78
52. A. Strasser, M. Skalicky, M. Hansalik, and A. Viidik The impact of environment in comparison with moderate physical exercise and dietary restriction on BDNF in the cerebral parietotemporal cortex of aged Sprague-Dawley rats Gerontology 52 2006 377 381
53. M. Uutela, J. Lindholm, V. Louhivuori, H. Wei, L.M. Louhivuori, A. Pertovaara, K. Akerman, E. Castrén, and M.L. Castrén Reduction of BDNF expression in Fmr1 knockout mice worsens cognitive deficits but improves hyperactivity and sensorimotor deficits Genes Brain Behav. 11 2012 513 523
54. M.W. Waung, B.E. Pfeiffer, E.D. Nosyreva, J.A. Ronesi, and K.M. Huber Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate Neuron 59 2008 84 97
55. E.G. Waterhouse, and B. Xu New insights into the role of brain-derived neurotrophic factor in synaptic plasticity Mol. Cell. Neurosci. 42 2009 81 89
56. D. Zamanillo, R. Sprengel, O. Hvalby, V. Jensen, N. Burnashev, A. Rozov, K.M. Kaiser, H.J. Köster, T. Borchardt, P. Worley, J. Lübke, M. Frotscher, P.H. Kelly, B. Sommer, P. Andersen, P.H. Seeburg, and B. Sakmann Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning Science 284 1999 1805 1811
57. Y. Zeng, X. Wang, Q. Wang, S. Liu, X. Hu, and S.M. McClintock Small molecules activating TrkB receptor for treating a variety of CNS disorders CNS Neurol. Disord. Drug Targets 12 2013 1066 1077
58. Y. Zeng, F. Lv, L. Li, H. Yu, M. Dong, and Q. Fu 7, 8-Dihydroxyflavone rescues spatial memory and synaptic plasticity in cognitively impaired aged rats J. Neurochem. 122 2012 800 811
59. Y. Zeng, Y. Liu, M. Wu, J. Liu, and Q. Hu Activation of TrkB by 7, 8-dihydroxyflavone prevents fear memory defects and facilitates amygdalar synaptic plasticity in aging J. Alzheimers Dis. 31 2012 765 768
60. Z. Zhang, X. Liu, J.P. Schroeder, C.B. Chan, M. Song, S.P. Yu, D. Weinshenker, and K. Ye 7, 8-Dihydroxyflavone prevents synaptic loss and memory deficits in a mouse model of Alzheimer's disease Neuropsychopharmacology 39 2014 638 650
61. M.G. Zhao, H. Toyoda, S.W. Ko, H.K. Ding, L.J. Wu, and M. Zhuo Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome J. Neurosci. 25 2005 7385 7392
62. C. Zuccato, and E. Cattaneo Brain-derived neurotrophic factor in neurodegenerative diseases Nat. Rev. Neurol. 5 2009 311 322