Deletion of FMR1 in purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in fragile X syndrome

Neuron

Volumn 47, Issue 3, 2005, Pages 339-352

  Koekkoek, S K E ^a   Yamaguchi, K ^b   Milojkovic, B A ^a   Dortland, B R ^a   Ruigrok, T J H ^a   Maex, R ^c   De Graaf, W ^a   Smit, A E ^a   VanderWerf, F ^a   Bakker, C E ^a   Willemsen, R ^a   Ikeda, T ^b   Kakizawa, S ^b   Onodera, K ^b   Nelson, D L ^d   Mientjes, E ^a   Joosten, M ^a   De Schutter, E ^c   Oostra, B A ^a   Ito, M ^b   De Zeeuw, C I ^a   more..

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONDITIONING; CONTROLLED STUDY; EYELID; FRAGILE X MENTAL RETARDATION 1 GENE; FRAGILE X SYNDROME; GENE; GENE DELETION; KNOCKOUT MOUSE; LEARNING DISORDER; LONG TERM DEPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SPINE; VELOCITY;

ANIMALS; CEREBELLUM; CONDITIONING, EYELID; DENDRITES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE DELETION; HUMANS; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MODELS, NEUROLOGICAL; NERVE FIBERS; NERVE TISSUE PROTEINS; PURKINJE CELLS; RNA-BINDING PROTEINS; STARTLE REACTION;

EID: 23044503253     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.07.005     Document Type: Article

References (65)

1. C.D. Aizenman, and D.J. Linden Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum J. Neurophysiol. 82 1999 1697 1709
2. C.D. Aizenman, and D.J. Linden Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons Nat. Neurosci. 3 2000 109 111
3. C.E. Bakker, Y. de Diego Otero, C. Bontekoe, P. Raghoe, T. Luteijn, A.T. Hoogeveen, B.A. Oostra, and R. Willemsen Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse Exp. Cell Res. 258 2000 162 170
4. J.J. Barski, K. Dethleffsen, and M. Meyer Cre recombinase expression in cerebellar Purkinje cells Genesis 28 2000 93 98
5. A.M. Batchelor, and J. Garthwaite Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway Nature 385 1997 74 77
6. M. Bravin, L. Morando, A. Vercelli, F. Rossi, and P. Strata Control of spine formation by electrical activity in the adult rat cerebellum Proc. Natl. Acad. Sci. USA 96 1999 1704 1709
7. V. Brown, P. Jin, S. Ceman, J.C. Darnell, W.T. O'Donnell, S.A. Tenenbaum, X. Jin, Y. Feng, K.D. Wilkinson, and J.D. Keene Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome Cell 107 2001 477 487
8. R. Cesa, L. Morando, and P. Strata Glutamate receptor delta2 subunit in activity-dependent heterologous synaptic competition J. Neurosci. 23 2003 2363 2370
9. L. Chen, and M. Toth Fragile X mice develop sensory hyperreactivity to auditory stimuli Neuroscience 103 2001 1043 1050
10. M. Coesmans, P.A. Smitt, D.J. Linden, R. Shigemoto, T. Hirano, Y. Yamakawa, A.M. van Alphen, C. Luo, J.N. van der Geest, and J.M. Kros Mechanisms underlying cerebellar motor deficits due to mGluR1-autoantibodies Ann. Neurol. 53 2003 325 336
11. M. Coesmans, J.T. Weber, C.I. De Zeeuw, and C. Hansel Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control Neuron 44 2004 691 700
12. T.A. Comery, J.B. Harris, P.J. Willems, B.A. Oostra, S.A. Irwin, I.J. Weiler, and W.T. Greenough Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits Proc. Natl. Acad. Sci. USA 94 1997 5401 5404
13. B.B. De Vries, A.M. van den Ouweland, S. Mohkamsing, H.J. Duivenvoorden, E. Mol, K. Gelsema, M. van Rijn, D.J. Halley, L.A. Sandkuijl, and B.A. Oostra Screening and diagnosis for the fragile X syndrome among the mentally retarded: an epidemiological and psychological survey. Collaborative Fragile X Study Group Am. J. Hum. Genet. 61 1997 660 667
14. C.I. De Zeeuw, J.C. Holstege, T.J. Ruigrok, and J. Voogd Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry J. Comp. Neurol. 284 1989 12 35
15. C.I. De Zeeuw, C. Hansel, F. Bian, S.K. Koekkoek, A.M. van Alphen, D.J. Linden, and J. Oberdick Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex Neuron 20 1998 495 508
16. C.I. De Zeeuw, Y. Elgersma, H.C. Hulscher, B.R. Dortland, R.A. Hensbroek, T.J. Ruigrok, and S.K.E. Koekkoek Response to comment on "Cerebellar LTD and Learning-Dependent Timing of Conditioned Eyelid Responses" Science 304 2004 211C
17. 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
18. C. Dobkin, A. Rabe, R. Dumas, A. El Idrissi, H. Haubenstock, and W.T. Brown Fmr1 knockout mouse has a distinctive strain-specific learning impairment Neuroscience 100 2000 423 429
19. Y.H. Fu, D.P. Kuhl, A. Pizzuti, M. Pieretti, J.S. Sutcliffe, S. Richards, A.J. Verkerk, J.J. Holden, R.G. Fenwick Jr., and S.T. Warren Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox Cell 67 1991 1047 1058
20. A. Gruart, A.M. Pastor, J.A. Armengol, and J.M. Delgado-Garcia Involvement of cerebellar cortex and nuclei in the genesis and control of unconditioned and conditioned eyelid motor responses Prog. Brain Res. 114 1997 511 528
21. Y. Gu, K.L. McIlwain, E.J. Weeber, T. Yamagata, B. Xu, B.A. Antalffy, C. Reyes, L. Yuva-Paylor, D. Armstrong, and H. Zoghbi Impaired conditioned fear and enhanced long-term potentiation in Fmr2 knock-out mice J. Neurosci. 22 2002 2753 2763
22. E.D. Haasdijk, A. Vlug, M.T. Mulder, and D. Jaarsma Increased apolipoprotein E expression correlates with the onset of neuronal degeneration in the spinal cord of G93A-SOD1 mice Neurosci. Lett. 335 2002 29 33
23. R.J. Hagerman, and P.J. Hagerman The fragile X premutation: into the phenotypic fold Curr. Opin. Genet. Dev. 12 2002 278 283
24. V.J. Hinton, W.T. Brown, K. Wisniewski, and R.D. Rudelli Analysis of neocortex in three males with the fragile X syndrome Am. J. Med. Genet. 41 1991 289 294
25. K.M. Huber, S.M. Gallagher, S.T. Warren, and M.F. Bear Altered synaptic plasticity in a mouse model of fragile X mental retardation Proc. Natl. Acad. Sci. USA 99 2002 7746 7750
26. R. Ichikawa, T. Miyazaki, M. Kano, T. Hashikawa, H. Tatsumi, K. Sakimura, M. Mishina, Y. Inoue, and M. Watanabe Distal extension of climbing fiber territory and multiple innervation caused by aberrant wiring to adjacent spiny branchlets in cerebellar Purkinje cells lacking glutamate receptor delta 2 J. Neurosci. 22 2002 8487 8503
27. S.A. Irwin, B. Patel, M. Idupulapati, J.B. Harris, R.A. Crisostomo, B.P. Larsen, F. Kooy, P.J. Willems, P. Cras, and P.B. Kozlowski Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination Am. J. Med. Genet. 98 2001 161 167
28. S.A. Irwin, M. Idupulapati, M.E. Gilbert, J.B. Harris, A.B. Chakravarti, E.J. Rogers, R.A. Crisostomo, B.P. Larsen, A. Mehta, and C.J. Alcantara Dendritic spine and dendritic field characteristics of layer V pyramidal neurons in the visual cortex of fragile-X knockout mice Am. J. Med. Genet. 111 2002 140 146
29. S. Kakizawa, M. Yamasaki, M. Watanabe, and M. Kano Critical period for activity-dependent synapse elimination in developing cerebellum J. Neurosci. 20 2000 4954 4961
30. M. Kano, K. Hashimoto, M. Watanabe, H. Kurihara, S. Offermanns, H. Jiang, Y. Wu, K. Jun, H.S. Shin, and Y. Inoue Phospholipase cbeta4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum Proc. Natl. Acad. Sci. USA 95 1998 15724 15729
31. L. Karachot, Y. Shirai, R. Vigot, T. Yamamori, and M. Ito Induction of long-term depression in cerebellar Purkinje cells requires a rapidly turned over protein J. Neurophysiol. 86 2001 280 289
32. R.M. Kelly, and P.L. Strick Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate J. Neurosci. 23 2003 8432 8444
33. G.T. Kenyon, J.F. Medina, and M.D. Mauk A mathematical model of the cerebellar-olivary system I: self-regulating equilibrium of climbing fiber activity J. Comput. Neurosci. 5 1998 17 33
34. J.J. Kim, and R.F. Thompson Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning Trends Neurosci. 20 1997 177 181
35. S.G. Kim, K. Ugurbil, and P.L. Strick Activation of a cerebellar output nucleus during cognitive processing Science 265 1994 949 951
36. S.K.E. Koekkoek, W.L. Den Ouden, G. Perry, S.M. Highstein, and C.I. De Zeeuw Monitoring kinetic and frequency-domain properties of eyelid responses in mice with magnetic distance measurement technique J. Neurophysiol. 88 2002 2124 2133
37. S.K. Koekkoek, H.C. Hulscher, B.R. Dortland, R.A. Hensbroek, Y. Elgersma, T.J. Ruigrok, and C.I. De Zeeuw Cerebellar LTD and learning-dependent timing of conditioned eyelid responses Science 301 2003 1736 1739
38. B. Laggerbauer, D. Ostareck, E.M. Keidel, A. Ostareck-Lederer, and U. Fischer Evidence that fragile X mental retardation protein is a negative regulator of translation Hum. Mol. Genet. 10 2001 329 338
39. H.C. Leiner, A.L. Leiner, and R.S. Dow Cognitive and language functions of the human cerebellum Trends Neurosci. 16 1993 444 447
40. Z. Li, Y. Zhang, L. Ku, K.D. Wilkinson, S.T. Warren, and Y. Feng The fragile X mental retardation protein inhibits translation via interacting with mRNA Nucleic Acids Res. 29 2001 2276 2283
41. D.J. Linden The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance Proc. Natl. Acad. Sci. USA 98 2001 14066 14071
42. I. Llano, A. Marty, C.M. Armstrong, and A. Konnerth Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices J. Physiol. 434 1991 183 213
43. M.D. Mauk, and N.H. Donegan A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum Learn. Mem. 4 1997 130 158
44. J.F. Medina, and M.D. Mauk Computer simulation of cerebellar information processing Nat. Neurosci. 3 Suppl. 2000 1205 1211
45. F.A. Middleton, and P.L. Strick Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function Science 266 1994 458 461
46. M. Migaud, P. Charlesworth, M. Dempster, L.C. Webster, A.M. Watabe, M. Makhinson, Y. He, M.F. Ramsay, R.G. Morris, and J.H. Morrison Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein Nature 396 1998 433 439
47. K.Y. Miyashiro, A. Beckel-Mitchener, T.P. Purk, K.G. Becker, T. Barret, L. Liu, S. Carbonetto, I.J. Weiler, W.T. Greenough, and J. Eberwine RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice Neuron 37 2003 417 431
48. M. Miyata, D. Okada, K. Hashimoto, M. Kano, and M. Ito Corticotropin-releasing factor plays a permissive role in cerebellar long-term depression Neuron 22 1999 763 775
49. D.M. Nielsen, W.J. Derber, D.A. McClellan, and L.S. Crnic Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome Brain Res. 927 2002 8 17
50. 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
51. R.D. Rudelli, W.T. Brown, K. Wisniewski, E.C. Jenkins, M. Laure-Kamionowska, F. Connell, and H.M. Wisniewski Adult fragile X syndrome. Clinico-neuropathologic findings Acta Neuropathol. (Berl.) 67 1985 289 295
52. K. Shibuki, H. Gomi, L. Chen, S. Bao, J.J. Kim, H. Wakatsuki, T. Fujisaki, K. Fujimoto, A. Katoh, and T. Ikeda Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice Neuron 16 1996 587 599
53. P. Strata, L. Morando, M. Bravin, and F. Rossi Dendritic spine density in Purkinje cells Trends Neurosci. 23 2000 198 198
54. T.M. Teune, J. van der Burg, J. van der Moer, J. Voogd, and T.J. Ruigrok Topography of cerebellar nuclear projections to the brain stem in the rat Prog. Brain Res. 124 2000 141 172
55. The Dutch-Belgian Fragile X Consortium Fmr1 knockout mice: A model to study fragile X mental retardation Cell 78 1994 23 33
56. G. Turner, T. Webb, S. Wake, and H. Robinson Prevalence of fragile X syndrome Am. J. Med. Genet. 64 1996 196 197
57. D. Van Dam, R. D'Hooge, E. Hauben, E. Reyniers, I. Gantois, C.E. Bakker, B.A. Oostra, R.F. Kooy, and P.P. De Deyn Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice Behav. Brain Res. 117 2000 127 136
58. J. Van Pelt, H.B. Uylings, R.W. Verwer, R.J. Pentney, and M.J. Woldenberg Tree asymmetry-a sensitive and practical measure for binary topological trees Bull. Math. Biol. 54 1992 759 784
59. C. Verheij, C.E. Bakker, E. de Graaff, J. Keulemans, R. Willemsen, A.J. Verkerk, H. Galjaard, A.J. Reuser, A.T. Hoogeveen, and B.A. Oostra Characterization and localization of the FMR-1 gene product associated with fragile X syndrome Nature 363 1993 722 724
60. A.J. Verkerk, M. Pieretti, J.S. Sutcliffe, Y.H. Fu, D.P. Kuhl, A. Pizzuti, O. Reiner, S. Richards, M.F. Victoria, and F.P. Zhang Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome Cell 65 1991 905 914
61. M. Vokaer, J.C. Bier, S. Elincx, T. Claes, P. Paquier, S. Goldman, E.J. Bartholome, and M. Pandolfo The cerebellum may be directly involved in cognitive functions Neurology 58 2002 967 970
62. S.S. Wang, W. Denk, and M. Hausser Coincidence detection in single dendritic spines mediated by calcium release Nat. Neurosci. 2 2000 1266 1273
63. I.J. Weiler, S.A. Irwin, A.Y. Klintsova, C.M. Spencer, A.D. Brazelton, K. Miyashiro, T.A. Comery, B. Patel, J. Eberwine, and W.T. Greenough Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation Proc. Natl. Acad. Sci. USA 94 1997 5395 5400
64. J. Xia, H.J. Chung, C. Wihler, R.L. Huganir, and D.J. Linden Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins Neuron 28 2000 499 510
65. C.H. Yeo, and G. Hesslow Cerebellum and conditioned reflexes Trends Cogn. Sci. 2 1998 322 331