Changes in synaptic morphology accompany actin signaling during LTP

Journal of Neuroscience

Volumn 27, Issue 20, 2007, Pages 5363-5372

  Chen, Lulu Y ^a   Rex, Christopher S ^a   Casale, Malcolm S ^a   Gall, Christine M ^a,b   Lynch, Gary ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cofilin; Dendritic spines; p21 activated kinase; Phosphorylation; Postsynaptic density; Synaptic plasticity

Indexed keywords

ACTIN; COFILIN; P21 ACTIVATED KINASE; POSTSYNAPTIC DENSITY PROTEIN 95;

ACTIN FILAMENT; ANIMAL TISSUE; ARTICLE; DENDRITIC SPINE; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE; THETA RHYTHM;

ACTINS; ANIMALS; DENDRITIC SPINES; LONG-TERM POTENTIATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPSES; TIME FACTORS;

EID: 34249055892     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0164-07.2007     Document Type: Article

References (60)

1. Aicardi G, Argilli E, Cappello S, Santi S, Riccio M, Thoenen H, Canossa M (2004) Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. Proc Natl Acad Sci USA 101:15788-15792.
2. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS (2001) Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239-257.
3. Balkowiec A, Katz DM (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10399-10407.
4. Boda B, Alberi S, Nikonenko I, Node-Langlois R, Jourdain P, Moosmayer M, Parisi-Jourdain L, Muller D (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J Neurosci 24:10816-10825.
5. Boda B, Nikonenko I, Alberi S, Muller D (2006) Central nervous system functions of PAK protein family: from spine morphogenesis to mental retardation. Mol Neurobiol 34:67-80.
6. Brakebusch C, Fassler R (2003) The integrin-actin connection, an eternal love affair. EMBO J 22:2324-2333.
7. Carlisle HJ, Kennedy MB (2005) Spine architecture and synaptic plasticity. Trends Neurosci 28:182-187.
8. Chen TJ, Gehler S, Shaw AE, Bamburg JR, Letourneau PC (2006) Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J Neurobiol 66:103-114.
9. Chong C, Tan L, Lim L, Manser E (2001) The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J Biol Chem 276:17347-17353.
10. Debanne D, Gahwiler BH, Thompson SM (1996) Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro. Proc Natl Acad Sci USA 93:11225-11230.
11. DeMali KA, Wennerberg K, Burridge K (2003) Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 15:572-582.
12. Fiala JC, Harris KM (2001) Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8:1-16.
13. Fifkova E, Van Harreveld A (1977) Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol 6:211-230.
14. Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847-854.
15. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447-460.
16. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y (2004) Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol 468:86-95.
17. Gehler S, Shaw AE, Sarmiere PD, Bamburg JR, Letourneau PC (2004) Brain-derived neurotrophic factor regulation of retinal growth cone filopodial dynamics is mediated through actin depolymerizing factor/cofilin. J Neurosci 24:10741-10749.
18. Geiger B, Bershadsky A, Pankov R, Yamada KM (2002) Transmembrane extracellular matrix- cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2:793-805.
19. Harris KM, Fiala JC, Ostroff L (2003) Structural changes at dendritic spine synapses during long-term potentiation. Philos Trans R Soc Lond B Biol Sci 358:745-748.
20. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, Zhang D, Chattarji S, Kirkwood A, Tonegawa S (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 42:773-787.
21. Hunt CA, Schenker LJ, Kennedy MB (1996) PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J Neurosci 16:1380-1388.
22. Ishizuka N, Cowan WM, Amaral DG (1995) A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J Comp Neurol 362:17-45.
23. Jain AK (1984) Fundamentals of digital image processing. Englewood Cliffs, NJ: Prentice Hall.
24. Jones DG, Calverley RK (1991) Perforated and non-perforated synapses in rat neocortex: three-dimensional reconstructions. Brain Res 556:247-258.
25. Juliano RL, Reddig P, Alahari S, Edin M, Howe A, Aplin A (2004) Integrin regulation of cell signalling and motility. Biochem Soc Trans 32:443-446.
26. Kramar EA, Lin B, Rex CS, Gall CM, Lynch G (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci USA 103:5579-5584.
27. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS (2004) Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci USA 101:16665-16670.
28. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.
29. Lee K, Oliver M, Schottler F, Creager R, Lynch G (1979) Ultrastructural effects of repetitive synaptic stimulation in the hippocampal slice preparation: a preliminary report. Exp Neurol 65:478-480.
30. Lee KS, Schottler F, Oliver M, Lynch G (1980) Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol 44:247-258.
31. Legate KR, Montanez E, Kudlacek O, Fassler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7:20-31.
32. Lin B, Kramar EA, Bi X, Brucher FA, Gall CM, Lynch G (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062-2069.
33. Lynch G, Baudry M (1984) The biochemistry of memory: a new and specific hypothesis. Science 224:1057-1063.
34. Matus A, Brinkhaus H, Wagner U (2000) Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 10:555-560.
35. Megias M, Emri Z, Freund TF, Gulyas AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540.
36. Muller D, Toni N, Buchs PA (2000) Spine changes associated with long-term potentiation. Hippocampus 10:596-604.
37. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759-767.
38. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559.
39. 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.
40. Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535-545.
41. Pavlidis P, Madison DV (1999) Synaptic transmission in pair recordings from CA3 pyramidal cells in organotypic culture. J Neurophysiol 81:2787-2797.
42. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL (2003) Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
43. 2+/calmodulin- dependent protein kinase II at the PSD. J Neurosci 23:11270-11278.
44. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512-2522.
45. Racz B, Weinberg RJ (2006) Spatial organization of cofilin in dendritic spines. Neuroscience 138:447-456.
46. Rex CS, Kramar EA, Colgin LL, Lin B, Gall CM, Lynch G (2005) Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J Neurosci 25:5956-5966.
47. Rex CS, Lauterborn JC, Lin CY, Kramar EA, Rogers GA, Gall CM, Lynch G (2006) Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J Neurophysiol 96:677-685.
48. Rex CS, Lin CY, Kramar EA, Chen LY, Gall CM, Lynch G (2007) Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27:3017-3029.
49. Ridley AJ (2001) Rho GTPases and cell migration. J Cell Sci 114:2713-2722.
50. Sassoe-Pognetto M, Utvik JK, Camoletto P, Watanabe M, Stephenson FA, Bredt DS, Ottersen OP (2003) Organization of postsynaptic density proteins and glutamate receptors in axodendritic and dendrodendritic synapses of the rat olfactory bulb. J Comp Neurol 463:237-248.
51. Scheff SW, Price DA, Hicks RR, Baldwin SA, Robinson S, Brackney C (2005) Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J Neurotrauma 22:719-732.
52. Shimono K, Kubota D, Brucher F, Taketani M, Lynch G (2002) Asymmetrical distribution of the Schaffer projections within the apical dendrites of hippocampal field CA1. Brain Res 950:279-287.
53. Sorra KE, Harris KM (1998) Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci 18:658-671.
54. Soule J, Messaoudi E, Bramham CR (2006) Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem Soc Trans 34:600-604.
55. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
56. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21:6245-6251.
57. Valtschanoff JG, Weinberg RJ (2001) Laminar organization of the NMDA receptor complex within the postsynaptic density. J Neurosci 21:1211-1217.
58. Wiesner S, Legate KR, Fassler R (2005) Integrin-actin interactions. Cell Mol Life Sci 62:1081-1099.
59. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
60. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.