Dynamic microtubules promote synaptic NMDA receptor-dependent spine enlargement

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Merriam, Elliott B ^a   Lumbard, Derek C ^a   Viesselmann, Chris ^a   Ballweg, Jason ^a   Stevenson, Matthew ^a   Pietila, Lauren ^a   Hu, Xindao ^a   Dent, Erik W ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL INVASION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC SPINE; HIPPOCAMPUS; LONG TERM POTENTIATION; MICROTUBULE ASSEMBLY; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; FEMALE; MALE; METABOLISM; MICROTUBULE; MOUSE; SYNAPSE;

ANIMALS; CELLS, CULTURED; DENDRITIC SPINES; FEMALE; MALE; MICE; MICROTUBULES; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 80855133563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027688     Document Type: Article

References (35)

1. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420: 788-794.
2. Grutzendler J, Kasthuri N, Gan WB, (2002) Long-term dendritic spine stability in the adult cortex. Nature 420: 812-816.
3. Yang G, Pan F, Gan WB, (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462: 920-924.
4. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M, (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457: 313-317.
5. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, et al. (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462: 915-919.
6. Frost NA, Shroff H, Kong H, Betzig E, Blanpied TA, (2010) Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67: 86-99.
7. Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GC, Kasai H, (2008) The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57: 719-729.
8. Okamoto K, Nagai T, Miyawaki A, Hayashi Y, (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7: 1104-1112.
9. Gu J, Firestein BL, Zheng JQ, (2008) Microtubules in dendritic spine development. J Neurosci 28: 12120-12124.
10. Hu X, Viesselmann C, Nam S, Merriam E, Dent EW, (2008) Activity-dependent dynamic microtubule invasion of dendritic spines. J Neurosci 28: 13094-13105.
11. Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, et al. (2009) Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61: 85-100.
12. Wagner W, Brenowitz SD, Hammer JA 3rd, (2011) Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol 13: 40-48.
13. Dent EW, Merriam EB, Hu X, (2011) The dynamic cytoskeleton: backbone of dendritic spine plasticity. Curr Opin Neurobiol 21: 174-181.
14. Lisman J, (2003) Long-term potentiation: outstanding questions and attempted synthesis. Philos Trans R Soc Lond B Biol Sci 358: 829-842.
15. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, et al. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29: 243-254.
16. Fortin DA, Davare MA, Srivastava T, Brady JD, Nygaard S, et al. (2010) Long-term potentiation-dependent spine enlargement requires synaptic Ca2+-permeable AMPA receptors recruited by CaM-kinase I. J Neurosci 30: 11565-11575.
17. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, et al. (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56: 640-656.
18. Patterson MA, Szatmari EM, Yasuda R, (2010) AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc Natl Acad Sci U S A 107: 15951-15956.
19. Bramham CR, (2008) Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18: 524-531.
20. Kerchner GA, Nicoll RA, (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9: 813-825.
21. Matsuzaki M, (2007) Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Res 57: 1-9.
22. Pi HJ, Otmakhov N, El Gaamouch F, Lemelin D, De Koninck P, et al. (2010) CaMKII control of spine size and synaptic strength: role of phosphorylation states and nonenzymatic action. Proc Natl Acad Sci U S A 107: 14437-14442.
23. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, et al. (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5: 599-609.
24. Yao J, Qi J, Chen G, (2006) Actin-dependent activation of presynaptic silent synapses contributes to long-term synaptic plasticity in developing hippocampal neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 26: 8137-8147.
25. Birkenfeld J, Nalbant P, Yoon SH, Bokoch GM, (2008) Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? Trends Cell Biol 18: 210-219.
26. Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu GY, et al. (2005) The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47: 85-100.
27. Kang MG, Guo Y, Huganir RL, (2009) AMPA receptor and GEF-H1/Lfc complex regulates dendritic spine development through RhoA signaling cascade. Proc Natl Acad Sci U S A 106: 3549-3554.
28. Guillaud L, Wong R, Hirokawa N, (2008) Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat Cell Biol 10: 19-29.
29. Schapitz IU, Behrend B, Pechmann Y, Lappe-Siefke C, Kneussel SJ, et al. (2010) Neuroligin 1 is dynamically exchanged at postsynaptic sites. J Neurosci 30: 12733-12744.
30. Kapitein LC, Yau KW, Gouveia SM, van der Zwan WA, Wulf PS, et al. (2011) NMDA Receptor Activation Suppresses Microtubule Growth and Spine Entry. J Neurosci 31: 8194-8209.
31. Kameyama K, Lee HK, Bear MF, Huganir RL, (1998) Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression. Neuron 21: 1163-1175.
32. Lee HK, Kameyama K, Huganir RL, Bear MF, (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21: 1151-1162.
33. Viesselmann C, Ballweg J, Lumbard D, Dent EW, (2011) Nucleofection and primary culture of embryonic mouse hippocampal and cortical neurons. J Vis Exps 47 http://www.jove.com/details.stp?id=2373 doi: 10.3791/2373.
34. Osumi N, Inoue T, (2001) Gene transfer into cultured mammalian embryos by electroporation. Methods 24: 35-42.
35. Kaech S, Banker G, (2006) Culturing hippocampal neurons. Nat Protoc 1: 2406-2415.