Mechanical coupling between transsynaptic N-cadherin adhesions and actin flow stabilizes dendritic spines

Molecular Biology of the Cell

Volumn 26, Issue 5, 2015, Pages 859-873

  Chazeau, Anaël ^a,b,d   Garcia, Mikael ^a,b,c   Czöndör, Katalin ^a,b   Perrais, David ^a,b   Tessier, Béatrice ^a,b   Giannone, Grégory ^a,b   Thoumine, Olivier ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CNRS   (France)

^c MINATEC   (France)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; F ACTIN; MYOSIN II; NERVE CELL ADHESION MOLECULE; CADHERIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; COMPUTER SIMULATION; CONTROLLED STUDY; DENDRITIC SPINE; EMBRYO; FILOPODIUM; FLOW RATE; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; SYNAPSE; ACTIN FILAMENT; ANIMAL; CELL CULTURE; METABOLISM; NERVE CELL; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CADHERINS; CELLS, CULTURED; DENDRITIC SPINES; HIPPOCAMPUS; MYOSIN TYPE II; NEURONS; RATS; SYNAPSES;

EID: 84923768802     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-06-1086     Document Type: Article

References (76)

1. Abe K, Chisaka O, Van Roy F, Takeichi M (2004). Stability of dendritic spines and synaptic contacts is controlled by alpha N-catenin. Nat Neurosci 7, 357-363.
2. Ackermann M, Matus A (2003). Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Neurosci 6, 1194-1200.
3. Arikkath J, Peng I-F, Ng YG, Israely I, Liu X, Ullian EM, Reichardt LF (2009). Delta-catenin regulates spine and synapse morphogenesis and function in hippocampal neurons during development. J Neurosci 29, 5435-5442.
4. Arikkath J, Reichardt LF (2008). Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci 31, 487-494.
5. Bard L, Boscher C, Lambert M, Mège R-M, Choquet D, Thoumine O (2008). A molecular clutch between the actin flow and N-cadherin adhesions drives growth cone migration. J Neurosci 28, 5879-5890.
6. Beaudoin GMJ, Schofield CM, Nuwal T, Zang K, Ullian EM, Huang B, Reichardt LF (2012). Afadin, a Ras/Rap effector that controls cadherin function, promotes spine and excitatory synapse density in the hippocampus. J Neurosci 32, 99-110.
7. Bloodgood BL, Sabatini BL (2005). Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310, 866-869.
8. 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.
9. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY (2002). A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99, 7877-7882.
10. Carlier MF, Criquet P, Pantaloni D, Korn ED (1986). Interaction of cytochalasin D with actin filaments in the presence of ADP and ATP. J Biol Chem 261, 2041-2050.
11. Chazeau A, Mehidi A, Nair D, Gautier JJ, Leduc C, Chamma I, Kage F, Kechkar A, Thoumine O, Rottner K, et al. (2014). Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion. EMBO J 33, 2745-2764.
12. Cingolani La, Goda Y (2008). Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9, 344-356.
13. Colicos M, Collins B, Sailor M, Goda Y (2001). Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107, 605-616.
14. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94, 5401-5404.
15. Czöndör K, Garcia M, Argento A, Constals A, Breillat C, Tessier B, Thoumine O (2013). Micropatterned substrates coated with neuronal adhesion molecules for high-content study of synapse formation. Nat Commun 4, 2252.
16. Czöndör K, Mondin M, Garcia M, Heine M, Frischknecht R, Choquet D, Sibarita J-B, Thoumine OR (2012). Unified quantitative model of AMPA receptor trafficking at synapses. Proc Natl Acad Sci USA 109, 3522-3527.
17. 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.
18. Fischer M, Kaech S, Knutti D, Matus A (1998). Rapid actin-based plasticity in dendritic spines. Neuron 20, 847-854.
19. 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.
20. Giannone G, Mège R-M, Thoumine O (2009). Multi-level molecular clutches in motile cell processes. Trends Cell Biol 19, 475-486.
21. Hodges JL, Newell-Litwa K, Asmussen H, Vicente-Manzanares M, Horwitz AR (2011). Myosin IIb activity and phosphorylation status determines dendritic spine and post-synaptic density morphology. PLoS One 6, e24149.
22. Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GCR, Kasai H (2008). The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57, 719-729.
23. Ibarretxe G, Perrais D, Jaskolski F, Vimeney A, Mulle C (2007). Fast regulation of axonal growth cone motility by electrical activity. J Neurosci 27, 7684-7695.
24. Inutsuka A, Goda M, Fujiyoshi Y (2009). Calyculin A-induced neurite retraction is critically dependent on actomyosin activation but not on polymerization state of microtubules. Biochem Biophys Res Commun 390, 1160-1166.
25. Izeddin I, Boulanger J, Racine V, Specht CG, Kechkar A, Nair D, Triller A, Choquet D, Dahan M, Sibarita JB (2012). Wavelet analysis for single molecule localization microscopy. Opt Express 20, 2081-2095.
26. Izeddin I, Specht CG, Lelek M, Darzacq X, Triller A, Zimmer C, Dahan M (2011). Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe. PLoS One 6, e15611.
27. Kaech S, Banker G (2006). Culturing hippocampal neurons. Nat Protoc 1, 2406-2415.
28. Kim IH, Racz B, Wang H, Burianek L, Weinberg R, Yasuda R, Wetsel WC, Soderling SH (2013). Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J Neurosci 33, 6081-6092.
29. Kolega J (2004). Phototoxicity and photoinactivation of blebbistatin in UV and visible light. Biochem Biophys Res Commun 320, 1020-1025.
30. Korobova F, Svitkina T (2010). Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 21, 165-176.
31. Koskinen M, Bertling E, Hotulainen R, Tanhuanpää K, Hotulainen P (2014). Myosin IIb controls actin dynamics underlying the dendritic spine maturation. Mol Cell Neurosci 61, 56-64.
32. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR (2004). Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279, 35557-35563.
33. Lambert M, Choquet D, Mège RM (2002). Dynamics of ligand-induced, Rac1-dependent anchoring of cadherins to the actin cytoskeleton. J Cell Biol 157, 469-479.
34. Lambert M, Thoumine O, Brevier J, Choquet D, Riveline D, Mège R-M (2007). Nucleation and growth of cadherin adhesions. Exp Cell Res 313, 4025-4040.
35. Maiden SL, Hardin J (2011). The secret life of α-catenin: moonlighting in morphogenesis. J Cell Biol 195, 543-552.
36. Mallavarapu A, Mitchison T (1999). Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146, 1097-1106.
37. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766.
38. Matsuzaki F, Mege RM, Jaffe SH, Friedlander DR, Gallin WJ, Goldberg JI, Cunningham BA, Edelman GM (1990). cDNAs of cell adhesion molecules of different specificity induce changes in cell shape and border formation in cultured S180 cells. J Cell Biol 110, 1239-1252.
39. Medeiros NA, Burnette DT, Forscher P (2006). Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8, 215-226.
40. 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.
41. Mitchison T, Kirschner M (1988). Cytoskeletal dynamics and nerve growth. Neuron 1, 761-772.
42. Mondin M, Labrousse V, Hosy E, Heine M, Tessier B, Levet F, Poujol C, Blanchet C, Choquet D, Thoumine O (2011). Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J Neurosci 31, 13500-13515.
43. Murakoshi H, Wang H, Yasuda R (2011). Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472, 100-104.
44. Murase S, Mosser E, Schuman EM (2002). Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91-105.
45. Mysore SP, Tai C-Y, Schuman EM (2007). Effects of N-cadherin disruption on spine morphological dynamics. Front Cell Neurosci 1, 1.
46. Okamoto K-I, 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.
47. Okamura K, Tanaka H, Yagita Y, Saeki Y, Taguchi A, Hiraoka Y, Zeng L-H, Colman DR, Miki N (2004). Cadherin activity is required for activity-induced spine remodeling. J Cell Biol 167, 961-972.
48. Okuda T, Yu LMY, Cingolani La, Kemler R, Goda Y (2007). beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proc Natl Acad Sci USA 104, 13479-13484.
49. Pilo Boyl P, Witke W (2014). Small, smaller... dendritic spine. EMBO J 33, 2737-2739.
50. Reymann A-C, Boujemaa-Paterski R, Martiel J-L, Guérin C, Cao W, Chin HF, De La Cruz EM, Théry M, Blanchoin L (2012). Actin network architecture can determine myosin motor activity. Science 336, 1310-1314.
51. Riehl R, Johnson K, Bradley R, Grunwald GB, Cornel E, Lilienbaum A, Holt CE (1996). Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837-848.
52. Rubio MD, Johnson R, Miller Ca, Huganir RL, Rumbaugh G (2011). Regulation of synapse structure and function by distinct myosin II motors. J Neurosci 31, 1448-1460.
53. Ryu J, Liu L, Wong TP, Wu DC, Burette A, Weinberg R, Wang YT, Sheng M (2006). A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49, 175-182.
54. Schubert V, Da Silva JS, Dotti CG (2006). Localized recruitment and activation of RhoA underlies dendritic spine morphology in a glutamate receptor-dependent manner. J Cell Biol 172, 453-467.
55. Schuman EM, Murase S (2003). Cadherins and synaptic plasticity: activity-dependent cyclin-dependent kinase 5 regulation of synaptic beta-catenin-cadherin interactions. Philos Trans R Soc Lond B Biol Sci 358, 749-756.
56. Star EN, Kwiatkowski DJ, Murthy VN (2002). Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5, 239-246.
57. Suter DM, Forscher P (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44, 97-113.
58. Takeichi M, Abe K (2005). Synaptic contact dynamics controlled by cadherin and catenins. Trends Cell Biol 15, 216-221.
59. Tanaka H, Shan W, Phillips GR, Arndt K, Bozdagi O, Shapiro L, Huntley GW, Benson DL, Colman DR (2000). Molecular modification of N-cadherin in response to synaptic activity. Neuron 25, 93-107.
60. Tashiro A, Yuste R (2004). Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol Cell Neurosci 26, 429-440.
61. Tatavarty V, Das S, Yu J (2012). Polarization of actin cytoskeleton is reduced in dendritic protrusions during early spine development in hippocampal neuron. Mol Biol Cell 23, 3167-3177.
62. Tatavarty V, Kim E-J, Rodionov V, Yu J (2009). Investigating sub-spine actin dynamics in rat hippocampal neurons with super-resolution optical imaging. PLoS One 4, e7724.
63. Thoumine O, Lambert M, Mège R-M, Choquet D (2006). Regulation of N-cadherin dynamics at neuronal contacts by ligand binding and cytoskeletal coupling. Mol Biol Cell 17, 862-875.
64. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M (2002). Cadherin regulates dendritic spine morphogenesis. Neuron 35, 77-89.
65. Uchida N, Honjo Y, Johnson KR, Wheelock MJ, Takeichi M (1996). The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol 135, 767-779.
66. Urban NT, Willig KI, Hell SW, Nagerl UV (2011). STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101, 1277-1284.
67. Vallotton P, Gupton SL, Waterman-Storer CM, Danuser G (2004). Simultaneous mapping of filamentous actin flow and turnover in migrating cells by quantitative fluorescent speckle microscopy. Proc Natl Acad Sci USA 101, 9660-9665.
68. Verma S, Han SP, Michael M, Gomez Ga, Yang Z, Teasdale RD, Ratheesh A, Kovacs EM, Ali RG, Yap AS (2012). A WAVE2-Arp2/3 actin nucleator apparatus supports junctional tension at the epithelial zonula adherens. Mol Biol Cell 23, 4601-4610.
69. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li XD, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD (2008). Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135, 535-548.
70. Wilson CA, Tsuchida MA, Allen GM, Barnhart EL, Applegate KT, Yam PT, Ji L, Keren K, Danuser G, Theriot JA (2010). Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465, 373-377.
71. Xie Z, Photowala H, Cahill ME, Srivastava DP, Woolfrey KM, Shum CY, Huganir RL, Penzes P (2008). Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7. J Neurosci 28, 6079-6091.
72. Yuste R, Bonhoeffer T (2004). Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5, 24-34.
73. Zhang X, Schaefer AW, Burnette DT, Schoonderwoert VT, Forscher P (2003). Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron 40, 931-944.
74. Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF (2005). A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25, 3379-3388.
75. Zhou Q, Homma KJ, Poo M (2004). Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749-757.
76. Ziv NE, Smith SJ (1996). Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102.