Impaired hippocampal long‐term potentiation in microtubule‐associated protein 1B‐deficient mice

Microtubule‐associated protein (MAP)1B‐heterozygous (MAP1B+/−) mice are deficient in the expression of MAP1B in the hippocampus, cerebellum, and olfactory cortex. Although MAP1B+/− mice showed half the normal levels of MAP1B protein, they had no measurable amounts of phosphorylated MAP1B. High‐frequency θ burst stimulation of Schaffer collateral‐CA1 axons in hippocampal slices from MAP1B+/− mice elicited long‐term potentiation (LTP) that decayed rapidly to baseline, in contrast to the non‐decremental LTP exhibited by age‐matched wild‐type slices. A separate group of MAP1B+/− and wild‐type slices was examined for a longer time course of 3 hr post‐tetanus in response to multiple high‐frequency stimulus trains that induced saturated LTP. MAP1B+/− slices showed marked reductions in both immediate post‐tetanic potentiation and LTP that decayed much more rapidly than that in wild‐type slices. The induction of LTP was associated with a rapid dephosphorylation of MAP1B within 5–15 min post‐tetanus, suggesting that the normal expression of MAP1B and conversion to a dephosphorylated state may be a cellular mediator of cytoskeletal alterations necessary for long‐term activity‐dependent synaptic plasticity. © 2005 Wiley‐Liss, Inc.

[1]  O. Reiner,et al.  Binding of microtubule-associated protein 1B to LIS1 affects the interaction between dynein and LIS1. , 2005, The Biochemical journal.

[2]  M. Heisenberg,et al.  Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila. , 2005, Molecular biology of the cell.

[3]  I. Fischer,et al.  Acute inactivation of MAP1b in growing sympathetic neurons destabilizes axonal microtubules. , 2005, Cell motility and the cytoskeleton.

[4]  T. Bliss,et al.  Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation(ltp): A serial section electron micrograph study in the dentate gyrus in the anaesthetised rat , 2004, Neuroscience.

[5]  Takeharu Nagai,et al.  Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity , 2004, Nature Neuroscience.

[6]  Yasuhiko Ohta,et al.  Hippocampal LTP Is Accompanied by Enhanced F-Actin Content within the Dendritic Spine that Is Essential for Late LTP Maintenance In Vivo , 2003, Neuron.

[7]  Kristen M Harris,et al.  Structural changes at dendritic spine synapses during long-term potentiation. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  R G M Morris,et al.  Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  Pascal Jourdain,et al.  LTP, memory and structural plasticity. , 2002, Current molecular medicine.

[10]  A. Alonso,et al.  Signaling Mechanisms Underlying Reversible, Activity-Dependent Dendrite Formation , 2002, Neuron.

[11]  J. Lisman,et al.  The molecular basis of CaMKII function in synaptic and behavioural memory , 2002, Nature Reviews Neuroscience.

[12]  N. Hirokawa,et al.  Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization , 2001, The Journal of cell biology.

[13]  H. Wässle,et al.  Map1b Is Required for Axon Guidance and Is Involved in the Development of the Central and Peripheral Nervous System , 2000, The Journal of cell biology.

[14]  E. Demandt,et al.  Perinatal Lethality of Microtubule-Associated Protein 1B-Deficient Mice Expressing Alternative Isoforms of the Protein at Low Levels , 2000, Molecular and Cellular Neuroscience.

[15]  N. Hirokawa,et al.  Defects in Axonal Elongation and Neuronal Migration in Mice with Disrupted tau and map1b Genes , 2000, The Journal of cell biology.

[16]  F. Engert,et al.  Dendritic spine changes associated with hippocampal long-term synaptic plasticity , 1999, Nature.

[17]  W. Zauner,et al.  The mouse and rat MAP1B genes: genomic organization and alternative transcription. , 1998, Genomics.

[18]  J. López-Barneo,et al.  NMDA-glutamate receptors regulate phosphorylation of dendritic cytoskeletal proteins in the hippocampus , 1997, Brain Research.

[19]  N. Hirokawa,et al.  Delayed Development of Nervous System in Mice Homozygous for Disrupted Microtubule-associated Protein 1B (MAP1B) Gene , 1997, The Journal of cell biology.

[20]  S. Kaech,et al.  Cytoskeletal Plasticity in Cells Expressing Neuronal Microtubule-Associated Proteins , 1996, Neuron.

[21]  E. Quinlan,et al.  Emergence of Activity-Dependent, Bidirectional Control of Microtubule-Associated Protein MAP2 Phosphorylation during Postnatal Development , 1996, The Journal of Neuroscience.

[22]  J. Ahringer,et al.  PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. , 1996, Journal of cell science.

[23]  R. Kucherlapati,et al.  Neuronal abnormalities in microtubule-associated protein 1B mutant mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Quinlan,et al.  Postsynaptic Mechanisms for Bidirectional Control of MAP2 Phosphorylation by Glutamate Receptors , 1996, Neuron.

[25]  Dominique Muller,et al.  Increased Phosphorylation of Ca/Calmodulin-dependent Protein Kinase II and Its Endogenous Substrates in the Induction of Long Term Potentiation (*) , 1995, The Journal of Biological Chemistry.

[26]  B. Riederer Differential phosphorylation of MAP1b during postnatal development of the cat brain , 1995, Journal of neurocytology.

[27]  D. Muller,et al.  Increased phosphorylation of Ca2+/calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long-term potentiation. , 1995, The Journal of biological chemistry.

[28]  J. Ávila,et al.  Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. , 1994, The International journal of developmental biology.

[29]  N. Hirokawa Microtubule organization and dynamics dependent on microtubule-associated proteins. , 1994, Current opinion in cell biology.

[30]  E. Raff The role of multiple tubulin isoforms in cellular microtubule function , 1994 .

[31]  J. Díaz-Nido,et al.  Heterogeneity in the Phosphorylation of Micro tubule‐Associated Protein MAP 1B During Rat Brair Development , 1993, Journal of neurochemistry.

[32]  J. Ávila,et al.  Depletion of casein kinase II by antisense oligonucleotide prevents neuritogenesis in neuroblastoma cells. , 1993, The EMBO journal.

[33]  K. Stratford,et al.  Presynaptic release probability influences the locus of long-term potentiation , 1992, Nature.

[34]  E. Fifková,et al.  Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. , 1992, International review of cytology.

[35]  J. Ávila,et al.  The distribution and phosphorylation of the microtubule-associated protein MAP 1B in growth cones , 1991, Journal of neurocytology.

[36]  Y. Ben-Ari,et al.  Rapid activation of hippocampal casein kinase II during long-term potentiation. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A. Matus Microtubule-associated proteins and neuronal morphogenesis , 1991, Journal of Cell Science.

[38]  B. McNaughton,et al.  Long‐term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content , 1991, Hippocampus.

[39]  P. Friedrich,et al.  Protein structure: The primary substrate for memory , 1990, Neuroscience.

[40]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[41]  M. Kirschner,et al.  Cytoskeletal dynamics and nerve growth , 1988, Neuron.

[42]  J. Sarvey,et al.  Blockade of norepinephrine-induced long-lasting potentiation in the hippocampal dentate gyrus by an inhibitor of protein synthesis , 1985, Brain Research.

[43]  J. Sarvey,et al.  Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  H. Schulman Phosphorylation of microtubule-associated proteins by a Ca2+/calmodulin- dependent protein kinase , 1984, The Journal of cell biology.

[45]  M. Krug,et al.  Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats , 1984, Brain Research Bulletin.

[46]  B L McNaughton,et al.  Long‐term synaptic enhancement and short‐term potentiation in rat fascia dentata act through different mechanisms , 1982, The Journal of physiology.

[47]  H. Haas,et al.  A simple perfusion chamber for the study of nervous tissue slices in vitro , 1979, Journal of Neuroscience Methods.

[48]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[49]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.