Loss of PSD-95 enrichment is not a prerequisite for spine retraction

Journal of Neuroscience

Volumn 31, Issue 34, 2011, Pages 12129-12138

  Woods, Georgia F ^a   Oh, Won Chan ^a   Boudewyn, Lauren C ^a   Mikula, Sarah K ^a   Zito, Karen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; RED FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; GENETIC TRANSFECTION; HIPPOCAMPUS; MALE; MORPHOLOGY; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PYRAMIDAL NERVE CELL; RAT; SPINE STABILIZATION; SYNAPSE;

ANIMALS; DENDRITIC SPINES; FEMALE; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PYRAMIDAL CELLS; RATS; RNA STABILITY; SYNAPSES; TRANSFECTION;

EID: 80052161487     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6662-10.2011     Document Type: Article

References (53)

1. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS (2001) Electron microscopic immunocytochemical detection of activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176-4181.
2. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
3. Fitzjohn SM, Palmer MJ, May JE, Neeson A, Morris SA, Collingridge GL (2001) A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J Physiol 537:421-430.
4. Gray NW, Weimer RM, Bureau I, Svoboda K (2006) Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol 4:e370.
5. Han K, Kim MH, Seeburg D, Seo J, Verpelli C, Han S, Chung HS, Ko J, Lee HW, Kim K, Heo WD, Meyer T, Kim H, Sala C, Choi SY, Sheng M, Kim E (2009) Regulated RalBP1 binding to RalA and PSD-95 controls AMPA receptor endocytosis and LTD. PLoS Biol 7:e1000187.
6. Harris KM, Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
7. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
8. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPARremoval underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.
9. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117-1124.
10. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced 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.
11. Bastrikova N, Gardner GA, Reece JM, Jeromin A, Dudek SM (2008) Synapse elimination accompanies functional plasticity in hippocampal neurons. Proc Natl Acad Sci U S A 105:3123-3127.
12. Becker N, Wierenga CJ, Fonseca R, Bonhoeffer T, Nägerl UV (2008) LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron 60:590-597.
13. Bhattacharyya S, Biou V, Xu W, Schlüter O, Malenka RC (2009) A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors. Nat Neurosci 12:172-181.
14. Blanpied TA, Kerr JM, Ehlers MD (2008) Structural plasticity with preserved topology in the postsynaptic protein network. Proc Natl Acad Sci U S A 105:12587-12592.
15. Chen X, Nelson CD, Li X, Winters CA, Azzam R, Sousa AA, Leapman RD, Gainer H, Sheng M, Reese TS (2011) PSD-95 is required to sustain the molecular organization of the postsynaptic density. J Neurosci 31:6329-6338.
16. Craven SE, El-Husseini AE, Bredt DS (1999) Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 22:497-509.
17. De Felipe J, Marco P, Fairén A, Jones EG (1997) Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb Cortex 7:619-634.
18. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L, Caroni P, Svoboda K (2006) Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49:861-875.
19. De Roo M, Klauser P, Mendez P, Poglia L, Muller D (2008) Activitydependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb Cortex 18:151-161.
20. Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176-4181.
21. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
22. Fitzjohn SM, Palmer MJ, May JE, Neeson A, Morris SA, Collingridge GL (2001) A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J Physiol 537:421-430.
23. Gray NW, Weimer RM, Bureau I, Svoboda K (2006) Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol 4:e370.
24. Han K, Kim MH, Seeburg D, Seo J, Verpelli C, Han S, Chung HS, Ko J, Lee HW, Kim K, Heo WD, Meyer T, Kim H, Sala C, Choi SY, Sheng M, Kim E (2009) Regulated RalBP1 binding to RalA and PSD-95 controls AMPA receptor endocytosis and LTD. PLoS Biol 7:e1000187.
25. Harris KM, Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
26. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
27. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPARremoval underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.
28. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117-1124.
29. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009.
30. Lawrence DG, Hopkins DA (1976) The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain 99:235-254.
31. Lee S, Lee K, Hwang S, Kim SH, Song WK, Park ZY, Chang S (2006) SPIN90/WISH interacts with PSD-95 and regulates dendritic spinogenesis via an N-WASP-independent mechanism. EMBO J 25:4983-4995.
32. Markus EJ, Petit TL (1987) Neocortical synaptogenesis, aging, and behavior: lifespan development in the motor-sensory system of the rat. Exp Neurol 96:262-278.
33. Marrs GS, Green SH, Dailey ME (2001) Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat Neurosci 4:1006-1013.
34. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
35. Okabe S, Kim HD, Miwa A, Kuriu T, Okado H (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 2:804-811.
36. Okabe S, Miwa A, Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21:6105-6114.
37. Pak DT, Yang S, Rudolph-Correia S, Kim E, Sheng M (2001) Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31:289-303.
38. Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, Kambampati V, Mains RE, Eipper BA (2001) The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29:229-242.
39. Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2:13.
40. Prange O, Murphy TH (2001) Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J Neurosci 21:9325-9333.
41. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232:232-235.
42. Roberts TF, Tschida KA, Klein ME, Mooney R (2010) Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463:948-952.
43. Sekino Y, Kojima N, Shirao T (2007) Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int 51:92-104.
44. Steiner P, Higley MJ, Xu W, Czervionke BL, Malenka RC, Sabatini BL (2008) Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 60:788-802.
45. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
46. Wise SP, Fleshman JW Jr, Jones EG (1979) Maturation of pyramidal cell form in relation to developing afferent and efferent connections of rat somatic sensory cortex. Neuroscience 4:1275-1297.
47. Woods G, Zito K (2008) Preparation of gene gun bullets and biolistic transfection of neurons in slice culture. J Vis Exp pii:675.
48. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, Zuo Y (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462:915-919.
49. Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920-924.
50. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H (2008) Principles of long-term dynamics of dendritic spines. J Neurosci 28:13592-13608.
51. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.
52. Zito K, Knott G, Shepherd GM, Shenolikar S, Svoboda K (2004) Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44:321-334.
53. Zuo Y, Yang G, Kwon E, Gan WB (2005) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436:261-265.