Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin

Journal of Neuroscience

Volumn 30, Issue 30, 2010, Pages 9984-9989

  Bozdagi, Ozlem ^a   Wang, Xiao Bin ^a   Nikitczuk, Jessica S ^a   Anderson, Tonya R ^a   Bloss, Erik B ^a   Radice, Glenn L ^b   Zhou, Qiang ^c   Benson, Deanna L ^a   Huntley, George W ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL DENSITY; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC SPINE; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MORPHOMETRICS; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RECORDING; SYNAPSE; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; CADHERINS; DENDRITIC SPINES; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, IMMUNOELECTRON; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; STATISTICS, NONPARAMETRIC; SYNAPSES;

EID: 77955401793     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1223-10.2010     Document Type: Article

References (40)

1. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF (2003) Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40:719-731.
2. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW (2000) Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28:245-259.
3. Bozdagi O, Valcin M, Poskanzer K, Tanaka H, Benson DL (2004) Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci 27:509-521.
4. Bozdagi O, Rich E, Tronel S, Sadahiro M, Patterson K, Shapiro ML, Alberini CM, Huntley GW, Salton SR (2008) The neurotrophininducible gene Vgf regulates hippocampal function and behavior through a brain-derived neurotrophic factor-dependent mechanism. J Neurosci 28:9857-9869.
5. Brock JH, Elste A, Huntley GW (2004) Distribution and injury-induced plasticity of cadherins in relationship to identified synaptic circuitry in adult rat spinal cord. J Neurosci 24:8806-8817. (Pubitemid 39362975)
6. Dodman NH, Karlsson EK, Moon-Fanelli A, Galdzicka M, Perloski M, Shuster L, Lindblad-Toh K, Ginns EI (2010) A canine chromosome 7 locus confers compulsive disorder susceptibility. Mol Psychiatry 15:8-10.
7. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89:4363-4367.
8. Elia LP, Yamamoto M, Zang K, Reichardt LF (2006) p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51:43-56.
9. Elste AM, Benson DL (2006) Structural basis for developmentally regulated changes in cadherin function at synapses. J Comp Neurol 495:324-335. (Pubitemid 43271476)
10. Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.
11. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neuron. Science 260:1661-1664.
12. Fukaya M, Kato A, Lovett C, Tonegawa S, WatanabeM (2003) Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc Natl Acad Sci U S A 100:4855-4860.
13. Gorski JA, Gomez LL, Scott JD, Dell'Acqua ML (2005) Association of an A-kinase-anchoring protein signaling scaffold with cadherin adhesion molecules in neurons and epithelial cells. Mol Biol Cell 16:3574-3590.
14. Gould TD, O'Donnell KC, Picchini AM, Dow ER, Chen G, Manji HK (2008) Generation and behavioral characterization of beta-catenin forebrain-specific conditional knock-out mice. Behav Brain Res 189:117-125.
15. 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.
16. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
17. Inoue A, Sanes JR (1997) Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276:1428-1431. (Pubitemid 27235414)
18. Jüngling K, Eulenburg V, Moore R, Kemler R, Lessmann V, Gottmann K (2006) N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons. J Neurosci 26:6968-6978.
19. Kadowaki M, Nakamura S, Machon O, Krauss S, Radice GL, Takeichi M (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22-33.
20. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825.
21. 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. (Pubitemid 43297870)
22. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706-13718.
23. Kostetskii I, Li J, Xiong Y, Zhou R, Ferrari VA, Patel VV, Molkentin JD, Radice GL (2005) Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res 96:346-354.
24. Lisman J, Raghavachari S (2006) A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006:re11.
25. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
26. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766. (Pubitemid 38833127)
27. Mendez P, De Roo M, Poglia L, Klauser P, Muller D (2010) N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol 189:589-600.
28. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32: 673-682.
29. Mysore SP, Tai CY, Schuman EM (2007) Effects of N-cadherin disruption on spine morphological dynamics. Front Cell Neurosci 1:1-14.
30. Nuriya M, Huganir RL (2006) Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 97:652-661.
31. 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.
32. Okamura K, Tanaka H, Yagita Y, Saeki Y, Taguchi A, Hiraoka Y, Zeng LH, Colman DR, Miki N (2004) Cadherin activity is required for activity-induced spine remodeling. J Cell Biol 167:961-972. (Pubitemid 39628118)
33. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
34. Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, Shan WS, Arndt K, Frank M, Gordon RE, Gawinowicz MA, Zhao Y, Colman DR (2001) The presynaptic particle web. ultrastructure, composition, dissolution, and reconstitution. Neuron 32:63-77.
35. Phillips GR, Florens L, Tanaka H, Khaing ZZ, Fidler L, Yates JR 3rd, Colman DR (2005) Proteomic comparison of two fractions derived from the transsynaptic scaffold. J Neurosci Res 81:762-775. (Pubitemid 41532142)
36. Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, McEwen BS, Morrison JH (2006) Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 16:313-320.
37. Radley JJ, Rocher AB, Rodriguez A, Ehlenberger DB, Dammann M, McEwen BS, Morrison JH, Wearne SL, Hof PR (2008) Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol 507:1141-1150. (Pubitemid 351214235)
38. Rodriguez A, Ehlenberger DB, Hof PR, Wearne SL (2006) Rayburst sampling, an algorithm for automated three-dimensional shape analysis from laser scanning microscopy images. Nat Protoc 1:2152-2161.
39. Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C, Sheng M, Passafaro M (2007) Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 54:461-477.
40. Shapiro L, Love J, Colman DR (2007) Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci 30:451-474. (Pubitemid 47218764)