Reversal of activity-mediated spine dynamics and learning impairment in a mouse model of Fragile X syndrome

European Journal of Neuroscience

Volumn 39, Issue 7, 2014, Pages 1130-1137

  Boda, Bernadett ^a   Mendez, Pablo ^a   Boury Jamot, Benjamin ^b   Magara, Fulvio ^b   Muller, Dominique ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Center for Psychiatric Neuroscience   (Switzerland)

Author keywords

LTD; LTP; Memory; Spinogenesis; Synaptic plasticity; Water maze

Indexed keywords

4 CARBOXY 2 METHYLPHENYLGLYCINE; DIPOTASSIUM BISPEROXO(5 HYDROXYPYRIDINE 2 CARBOXYL)OXOVANADATE; ENZYME INHIBITOR; FRAGILE X MENTAL RETARDATION PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG; FMR1 PROTEIN, MOUSE; METABOTROPIC RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; FRAGILE X SYNDROME; HIPPOCAMPUS; IMAGING; KNOCKOUT MOUSE; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MOUSE; MOUSE MODEL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; COGNITION; GENETICS; HIPPOCAMPAL CA1 REGION; MAZE TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CELLS, CULTURED; COGNITION; DENDRITIC SPINES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84898723842     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12488     Document Type: Article

References (41)

1. Alvarez, V.A., Ridenour, D.A. & Sabatini, B.L. (2006) Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J. Neurosci., 26, 7820-7825.
2. Anwyl, R. (2009) Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology, 56, 735-740.
3. Auerbach, B.D. & Bear, M.F. (2010) Loss of the fragile X mental retardation protein decouples metabotropic glutamate receptor dependent priming of long-term potentiation from protein synthesis. J. Neurophysiol., 104, 1047-1051.
4. Bhattacharya, A., Kaphzan, H., Alvarez-Dieppa, A.C., Murphy, J.P., Pierre, P. & Klann, E. (2012) Genetic removal of p70 S6 kinase 1 corrects molecular, synaptic, and behavioral phenotypes in fragile X syndrome mice. Neuron, 76, 325-337.
5. Cao, C., Rioult-Pedotti, M.S., Migani, P., Yu, C.J., Tiwari, R., Parang, K., Spaller, M.R., Goebel, D.J. & Marshall, J. (2013) Impairment of TrkB-PSD-95 signaling in Angelman syndrome. PLoS Biol., 11, e1001478.
6. Caroni, P., Donato, F. & Muller, D. (2012) Structural plasticity upon learning: regulation and functions. Nat. Rev. Neurosci., 13, 478-490.
7. Chen, L.Y., Rex, C.S., Babayan, A.H., Kramar, E.A., Lynch, G., Gall, C.M. & Lauterborn, J.C. (2010) Physiological activation of synaptic Rac>PAK (p-21 activated kinase) signaling is defective in a mouse model of fragile X syndrome. J. Neurosci., 30, 10977-10984.
8. Comery, T.A., Harris, J.B., Willems, P.J., Oostra, B.A., Irwin, S.A., Weiler, I.J. & Greenough, W.T. (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. USA, 94, 5401-5404.
9. Cruz-Martin, A., Crespo, M. & Portera-Cailliau, C. (2010) Delayed stabilization of dendritic spines in fragile X mice. J. Neurosci., 30, 7793-7803.
10. Cuesto, G., Enriquez-Barreto, L., Carames, C., Cantarero, M., Gasull, X., Sandi, C., Ferrus, A., Acebes, A. & Morales, M. (2011) Phosphoinositide-3-kinase activation controls synaptogenesis and spinogenesis in hippocampal neurons. J. Neurosci., 31, 2721-2733.
11. De Roo, M., Klauser, P., Mendez, P., Poglia, L. & Muller, D. (2008a) Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb. Cortex, 18, 151-161.
12. De Roo, M., Klauser, P. & Muller, D. (2008b) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol., 6, e219.
13. Dolan, B.M., Duron, S.G., Campbell, D.A., Vollrath, B., Rao, B.S., Ko, H.Y., Lin, G.G., Govindarajan, A., Choi, S.Y. & Tonegawa, S. (2013) Rescue of fragile X syndrome phenotypes in Fmr1 KO mice by the small-molecule PAK inhibitor FRAX486. Proc. Natl. Acad. Sci. USA, 110, 5671-5676.
14. Dolen, G., Osterweil, E., Rao, B.S., Smith, G.B., Auerbach, B.D., Chattarji, S. & Bear, M.F. (2007) Correction of fragile X syndrome in mice. Neuron, 56, 955-962.
15. Dubos, A., Combeau, G., Bernardinelli, Y., Barnier, J.V., Hartley, O., Gaertner, H., Boda, B. & Muller, D. (2012) Alteration of synaptic network dynamics by the intellectual disability protein PAK3. J. Neurosci., 32, 519-527.
16. Gross, C., Nakamoto, M., Yao, X., Chan, C.B., Yim, S.Y., Ye, K., Warren, S.T. & Bassell, G.J. (2010) Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome. J. Neurosci., 30, 10624-10638.
17. Grossman, A.W., Elisseou, N.M., McKinney, B.C. & Greenough, W.T. (2006) Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Brain Res., 1084, 158-164.
18. Hayashi, M.L., Rao, B.S., Seo, J.S., Choi, H.S., Dolan, B.M., Choi, S.Y., Chattarji, S. & Tonegawa, S. (2007) Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc. Natl. Acad. Sci. USA, 104, 11489-11494.
19. Hemmings, B.A. & Restuccia, D.F. (2012) PI3K-PKB/Akt pathway. Cold Spring Harb. Perspect. Biol., 4, a011189.
20. Hu, H., Qin, Y., Bochorishvili, G., Zhu, Y., van Aelst, L. & Zhu, J.J. (2008) Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J. Neurosci., 28, 7847-7862.
21. Huber, K.M., Gallagher, S.M., Warren, S.T. & Bear, M.F. (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA, 99, 7746-7750.
22. Irwin, S.A., Galvez, R. & Greenough, W.T. (2000) Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex, 10, 1038-1044.
23. Jaworski, J., Spangler, S., Seeburg, D.P., Hoogenraad, C.C. & Sheng, M. (2005) Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J. Neurosci., 25, 11300-11312.
24. Jurado, S., Benoist, M., Lario, A., Knafo, S., Petrok, C.N. & Esteban, J.A. (2010) PTEN is recruited to the postsynaptic terminal for NMDA receptor-dependent long-term depression. EMBO J., 29, 2827-2840.
25. Krueger, D.D. & Bear, M.F. (2011) Toward fulfilling the promise of molecular medicine in fragile X syndrome. Annu. Rev. Med., 62, 411-429.
26. Lauterborn, J.C., Rex, C.S., Kramar, E., Chen, L.Y., Pandyarajan, V., Lynch, G. & Gall, C.M. (2007) Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J. Neurosci., 27, 10685-10694.
27. Mao, L., Jia, J., Zhou, X., Xiao, Y., Wang, Y., Mao, X., Zhen, X., Guan, Y., Alkayed, N.J. & Cheng, J. (2013) Delayed administration of a PTEN inhibitor BPV improves functional recovery after experimental stroke. Neuroscience, 231, 272-281.
28. Meredith, R.M., Holmgren, C.D., Weidum, M., Burnashev, N. & Mansvelder, H.D. (2007) Increased threshold for spike-timing-dependent plasticity is caused by unreliable calcium signaling in mice lacking fragile X gene FMR1. Neuron, 54, 627-638.
29. Michalon, A., Sidorov, M., Ballard, T.M., Ozmen, L., Spooren, W., Wettstein, J.G., Jaeschke, G., Bear, M.F. & Lindemann, L. (2012) Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Neuron, 74, 49-56.
30. Mientjes, E.J., Nieuwenhuizen, I., Kirkpatrick, L., Zu, T., Hoogeveen-Westerveld, M., Severijnen, L., Rife, M., Willemsen, R., Nelson, D.L. & Oostra, B.A. (2006) The generation of a conditional Fmr1 knock out mouse model to study Fmrp function in vivo. Neurobiol. Dis., 21, 549-555.
31. Osterweil, E.K., Kind, P.C. & Bear, M.F. (2012) Lifting the mood on treating fragile X. Biol. Psychiat., 72, 895-897.
32. Osterweil, E.K., Chuang, S.C., Chubykin, A.A., Sidorov, M., Bianchi, R., Wong, R.K. & Bear, M.F. (2013) Lovastatin corrects excess protein synthesis and prevents epileptogenesis in a mouse model of fragile X syndrome. Neuron, 77, 243-250.
33. Pan, F., Aldridge, G.M., Greenough, W.T. & Gan, W.B. (2010) Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome. Proc. Natl. Acad. Sci. USA, 107, 17768-17773.
34. Pfeiffer, B.E. & Huber, K.M. (2007) Fragile X mental retardation protein induces synapse loss through acute postsynaptic translational regulation. J. Neurosci., 27, 3120-3130.
35. Pfeiffer, B.E., Zang, T., Wilkerson, J.R., Taniguchi, M., Maksimova, M.A., Smith, L.N., Cowan, C.W. & Huber, K.M. (2010) Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron, 66, 191-197.
36. Schmid, A.C., Byrne, R.D., Vilar, R. & Woscholski, R. (2004) Bisperoxovanadium compounds are potent PTEN inhibitors. FEBS Lett., 566, 35-38.
37. Scotto-Lomassese, S., Nissant, A., Mota, T., Neant-Fery, M., Oostra, B.A., Greer, C.A., Lledo, P.M., Trembleau, A. & Caille, I. (2011) Fragile X mental retardation protein regulates new neuron differentiation in the adult olfactory bulb. J. Neurosci., 31, 2205-2215.
38. Seese, R.R., Babayan, A.H., Katz, A.M., Cox, C.D., Lauterborn, J.C., Lynch, G. & Gall, C.M. (2012) LTP induction translocates cortactin at distant synapses in wild-type but not Fmr1 knock-out mice. J. Neurosci., 32, 7403-7413.
39. Sharma, A., Hoeffer, C.A., Takayasu, Y., Miyawaki, T., McBride, S.M., Klann, E. & Zukin, R.S. (2010) Dysregulation of mTOR signaling in fragile X syndrome. J. Neurosci., 30, 694-702.
40. Stoppini, L., Buchs, P.A. & Muller, D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Meth., 37, 173-182.
41. Tang, S.J., Reis, G., Kang, H., Gingras, A.C., Sonenberg, N. & Schuman, E.M. (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl. Acad. Sci. USA, 99, 467-472.